Survival after liver transplantation: Is racial disparity inevitable?

Survival After Liver Transplantation:Is Racial Disparity Inevitable?

Tae Hoon Lee,1 Nilay Shah,2 Rachel A. Pedersen,3 Walter K. Kremers,3 Charles B. Rosen,1

Goran B. Klintmalm,4 and W. Ray Kim1,2

Previous analyses have reported that minority patients undergoing orthotopic liver trans-plantation (OLT) have poorer survival than Caucasian recipients. The reason for this dis-parity is unclear. We examined whether racial differences in survival exist at select academicOLT centers. OLT recipients from 4 academic centers were prospectively enrolled in 2multicenter databases. Data including demographics, liver disease diagnosis, and post-OLTfollow-up were obtained for 2823 (135 African, 2448 Caucasian, and 240 other race) adultpatients undergoing primary OLT between 1985 and 2000. The survival of patients andgrafts after OLT was compared across race. The Kaplan-Meier estimates for 1-year recipientsurvival were 90.8% [95% confidence interval (CI): 86.0-95.9] for African Americans,86.5% (95% CI: 85.1-87.9) for Caucasians, and 84.4% (95% CI: 79.8-89.2) for other races.The 5-year recipient survival probability was 69.2% (95% CI: 60.1-79.7) for African Amer-icans, 72.2% (95% CI: 70.1-74.4) for Caucasians, and 67.5% (95% CI: 60.5-75.3) for otherraces. The 10-year recipient survival probability for African Americans was 54.4% (95% CI:41.1-72.1), for Caucasians 50.7% (95% CI: 46.4-55.3), and for other races 55.7% (95% CI:41.5-74.8). There was no difference in patient survival (P � 0.162) or graft survival (P �0.582) among racial groups. A multivariable proportional hazards model confirmed theabsence of an association between race and post-OLT survival after adjustments for age,gender, total bilirubin, creatinine, prothrombin time, and diagnosis. Conclusion: These datademonstrate that as a proof of principle, minority OLT recipients should not necessarilyexpect an OLT outcome inferior to that of Caucasians. (HEPATOLOGY 2007;46:1491-1497.)

There has been a controversy concerning whetherthe race of recipients affects patient and graft sur-vival following orthotopic liver transplantation

(OLT). After an initial report from the University ofPittsburgh in 1989,1 a number of studies have indicatedpoorer survival for African American recipients in com-parison with Caucasian recipients.2-5 Other published

studies have suggested no racial differences in outcomefollowing OLT.6-10 The discrepancy between these stud-ies may be explained by small sample sizes that lacked thepower to detect meaningful differences between races orinadequate controls for confounding factors, such as thefact that recipient race may have been only a surrogate forother factors (for example, comorbidity or more advancedliver failure) that affect the outcome more directly.

There may be several mechanisms by which race maybe associated with outcome after OLT. Some may have abiological basis, such as immunologic disparities betweendonors and recipients of different racial backgrounds andgenetic differences in the pharmacokinetics or pharmaco-dynamics of immunosuppressant agents.2,11-13 Alterna-tively, they may be socioeconomic, such as inadequatehealth insurance delaying presentation for OLT in minor-ity patients, socioeconomic status affecting the affordabil-ity or choice of immunosuppressive agents, and culturalbeliefs that may affect the acceptance of organ transplan-tation or posttransplant care.14-16 Because more than oneof these factors may be in effect, it may be difficult todisentangle these complex relationships.

Abbreviations: CI, confidence interval; HBV, hepatitis B virus; HCC, hepato-cellular carcinoma; HR, hazard ratio; MELD, model for end-stage liver disease;OLT, orthotopic liver transplantation; UNOS, United Network for Organ Shar-ing.

From the 1William J. von Liebig Transplant Center, 2Division of Health CarePolicy and Research, and 3Division of Biostatistics, Mayo Clinic College of Medi-cine, Rochester, MN; and 4Baylor Transplant Institute, Baylor University MedicalCenter, Dallas, TX.

Received February 1, 2007; accepted May 19, 2007.Supported by grants from the National Institute of Diabetes and Digestive and

Kidney Diseases (DK-34238 and DK-61617).Address reprint requests to: W. Ray Kim, M.D., Division of Gastroenterology and

Hepatology (PL 6), 200 1st Street SW, Rochester, MN 55905. E-mail:[email protected]; fax: 507-538-3974.

Copyright © 2007 by the American Association for the Study of Liver Diseases.Published online in Wiley InterScience (www.interscience.wiley.com).DOI 10.1002/hep.21830Potential conflict of interest: Nothing to report.

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Recently, Nair et al.17 analyzed data from the UnitedNetwork for Organ Sharing (UNOS) and reported thatbeing African or Asian American was an independent riskfactor for poorer outcome after OLT in comparison withbeing Caucasian. In a follow-up report evaluating the in-fluence of socioeconomic status on OLT outcome, it wasconcluded that race was still a strong independent predic-tor of survival, even though socioeconomic status hadsome effect on survival.18 These data are strong becausethey captured all OLT recipients in the nation. However,one important confounding variable was not taken intoaccount in these analyses: the effect of the hospital orregion in which OLT was performed. For example, ifminority patients are aggregated at OLT centers with in-ferior outcomes, it would lead to a spurious result thatrace is responsible for the poor outcome when, in fact, theproblem may be that minority patients have limited accessto centers with optimal OLT outcomes.

In this study, we consider racial differences in survivalafter OLT, using data from selected, high-volume, aca-demic OLT centers after adjusting for other factors thataffect post-OLT survival. Our data show no differences inOLT outcome among different races at these select cen-ters, suggesting that disparities seen in the nationwidesetting are not inevitable.

Materials and Methods

Data Source and Elements. This study was based on2 National Institutes of Health–sponsored multicenterOLT databases. First, the National Institute of Diabetesand Digestive and Kidney Disease Liver TransplantationDatabase prospectively enrolled patients who underwentOLT between 1985 and 1994 at the Mayo Clinic (Roch-ester, MN), the University of California at San Francisco(San Francisco, CA), and the University of Nebraska(Omaha, NE). Second, the Model for End-Stage LiverDisease (MELD) Study Group Database included OLTrecipients between 1994 and 2000 from the Mayo Clinicand Baylor University (Dallas, TX). From these data-bases, all adult (age � 18 years) primary liver transplantrecipients were included in this analysis.

In both databases, the recipient race was designated bythe healthcare provider (physician or transplant coordina-tor) and categorized as Caucasian, African, or other race.In addition to race, pre-OLT variables that may have apotential impact on post-OLT survival were extracted ascovariates in the analysis. These included demographic(age and gender), clinical (liver disease diagnosis), andlaboratory data (MELD components at the time of theinitial evaluation and OLT). Liver disease diagnoses werecoded as fulminant hepatic failure, cancer (primary liver

malignancy), alcoholic liver disease, cholestatic liver dis-ease, hepatitis B, hepatitis C, and other. The causes offulminant hepatic failure were extracted if this informa-tion was available.

Statistical Methods. For a comparison of the baselinecharacteristics across the racial groups, the Wilcoxon-Rank sum test was used for continuous variables, and achi-square test was used for categorical variables. Labora-tory data at the time of the initial evaluation were used forthis comparison. Survival was calculated with the lastknown follow-up date in comparison with the date ofOLT. Patients who were alive on the last day of follow-upwere censored at that time. The Kaplan-Meier methodwas used to estimate recipient and graft survival aftertransplant by race. The proportional hazards regressionanalysis was used to examine the impact of race on arecipient’s survival, while stratifying on the center. Co-variates to adjust for differences in baseline characteristicsincluded age, gender, liver disease diagnosis, and labora-tory data to represent the severity of liver disease at thetime of OLT. A P value less than 0.05 was used for statis-tical significance in all analyses.

Results

Recipient Characteristics. A total of 2823 OLT re-cipients were included in this study after the exclusion of28 patients (1.0%) whose race was not reported. Asshown in Table 1, 135 (4.8%) recipients were African,2448 (86.7%) were Caucasian, and 240 (8.5%) were ofother races, including Asian and Hispanic. African Amer-ican recipients were significantly younger than Cauca-sians (P � 0.01). There were more female recipientsamong African Americans than other groups (P � 0.01).Overall, hepatitis C was the commonest single diseaseentity. In comparison with Caucasians, the proportion ofAfrican Americans with fulminant (P � 0.01) and otherliver diseases (P � 0.02) was higher, whereas the propor-tion with alcoholic (P � 0.047) and cholestatic liver dis-eases (P � 0.02) was lower. With respect to other races,the frequency of hepatic malignancy (P � 0.01) and hep-atitis B virus (HBV; P � 0.01) was higher and the fre-quency of alcoholic (P � 0.01) and cholestatic liverdiseases (P � 0.01) was lower in comparison with Cau-casians.

Table 2 compares laboratory data at the time of theinitial evaluation among the 3 racial groups. Of the pa-tients with nonfulminant liver disease, African Americanshad significantly higher serum total bilirubin (P � 0.03),creatinine (P � 0.045), and prothrombin time (P � 0.01)in comparison with Caucasians. This trend for AfricanAmerican patients presenting with more advanced liver

1492 LEE ET AL. HEPATOLOGY, November 2007

disease was not seen with fulminant disease. AfricanAmerican patients with fulminant liver failure had signif-icantly lower total bilirubin than Caucasians (P � 0.01).The etiology of fulminant hepatic failure was most com-monly unknown (n � 49), followed by viral hepatitis(n � 42), drug toxicity (n � 7), and autoimmune andother miscellaneous causes. No apparent pattern wasfound among the racial groups (data not shown).

Survival of OLT Recipients by Race. Figure 1 showspatient and graft survival for the 3 racial groups. TheKaplan-Meier estimates for 1-year, 5-year, and 10-yearpatient survival was 86.5%, 71.6%, and 50.8%, respec-tively, and the graft survival was 81.3%, 66.3%, and46.9%, respectively. There was no difference among theracial groups for patient survival (P � 0.16) or graft sur-vival (P � 0.58). In particular, patient survival betweenCaucasian and African American patients overlapped ex-tensively.

Figure 2 compares the survival of patients by race withfulminant and nonfulminant liver diseases. The 1-year,5-year, and 10-year survival of patients with nonfulmi-nant disease was 87.1%, 71.7%, and 49.9%, respectively.Among patients with fulminant liver disease, the 1-year,5-year, and 10-year survival was 77.2%, 68.9%, and63.6%, respectively. Overall, the patients with fulminantliver disease had survival results comparable to those ofthe patients with nonfulminant disease (P � 0.78). Moreimportantly, in neither group was there any differenceamong the racial groups in patient survival (P � 0.74 and0.13 for fulminant and nonfulminant diagnoses, respec-tively).

The univariate proportional hazards regression analysisshowed that age [hazard ratio (HR) � 1.25], female gen-der (HR � 0.81), serum creatinine (HR � 1.05), livercancer (HR � 1.54), alcoholic liver disease (HR � 1.27),viral hepatitis (HR � 1.57), and cholestatic liver disease

Table 1 Recipients’ Characteristics by Race

Caucasian African Other Total

Total number 2448 (86.7%) 135 (4.8%) 240 (8.5%) 2823Center

A 1407 (89.9%) 101 (6.5%) 57 (3.6%) 1565 (55.4%)B 630 (89.9%) 7 (1.0%) 64 (9.1%) 701 (24.8%)C 189 (87.5%) 7 (3.2%) 20 (9.3%) 216 (7.7%)D 222 (65.1%) 20 (5.9%) 99 (29.0%) 341 (12.1%)

Age (years)† 49.8 � 10.9 43.1 � 11.7* 48.2 � 11.0 49.3 � 11.0Male gender 1351 (55.2%) 59 (43.7%)* 126 (52.5%) 1536 (54.4%)Diagnosis group

Fulminant hepatic failure 100 (4.1%) 20 (14.8%)* 14 (5.8%) 134 (4.7%)Cancer 91 (3.7%) 2 (1.5%) 18 (7.5%)* 111 (3.9%)Alcoholic liver disease 326 (13.3%) 10 (7.4%)* 17 (7.1%)* 353 (12.5%)Cholestatic disease 605 (24.7%) 21 (15.6%)* 30 (12.5%)* 656 (23.2%)Hepatitis B virus 109 (4.5%) 5 (3.7%) 42 (17.5%)* 156 (5.5%)Hepatitis C virus 573 (23.4%) 29 (21.5%) 67 (27.9%) 669 (23.7%)Other 644 (26.3%) 48 (35.6%)* 52 (21.7%) 744 (26.4%)

* P � 0.05(reference: Caucasian).† Mean � the standard deviation.

Table 2 Recipients’ Characteristics at the Time of the Initial Evaluation by Race (Median and Interquartile Range)

Nonfulminant Hepatic Failure

Caucasian(n � 2348)

African(n � 115)

Other(n � 226)

Total bilirubin (mg/dL) 2.9 (1.8-5.9) 4.1 (1.7-10.1)* 2.9 (1.6-6.1)Creatinine (mg/dL) 0.9 (0.8-1.2) 1.0 ( 0.8-1.4)* 0.9 (0.8-1.2)Prothrombin time (seconds) 13.7 (12.4-15.2) 14.2 (12.8-17.3)* 13.8 (12.6-15.5)

Fulminant Hepatic Failure

Caucasian(n � 100)

African(n � 20)

Other(n � 14)

Total bilirubin (mg/dL) 25.6 (17.7-31.0) 18.8 (13.9-20.7)* 17.4 (3.6-22.7)Creatinine (mg/dL) 1.3 (0.8-2.6) 1.0 (0.8-1.2) 0.9 (0.7-1.0)Prothrombin time (seconds) 25.0 (18.5-34.4) 26.0 (17.5-47.8) 26.5 (13.3-27.9)

* P � 0.05 (reference: Caucasian).

HEPATOLOGY, Vol. 46, No. 5, 2007 LEE ET AL. 1493

(HR � 0.47) were significantly associated with patientsurvival (Table 3). In agreement with Fig. 2, fulminantliver disease was not associated with an increased risk ofdeath. Other race was associated with an increased risk ofdeath (HR � 1.36, P � 0.03) in comparison with Cau-casian race, whereas African race was not (HR � 0.90,P � 0.53).

Table 4 summarizes a multivariable proportional haz-ards model correlating pre-OLT characteristics with post-OLT survival among recipients with nonfulminant liverdisease. After adjustments for age, gender, diagnosis, andbaseline laboratory data, there was no association betweenAfrican race (HR � 0.85, P � 0.42) or other race (HR �1.25, P � 0.13) and post-OLT survival. In the samemodel, compared with recipients with viral hepatitis, re-cipients with cholestatic disease (HR � 0.39, P � 0.01)and other liver disease categories (HR � 0.69, P � 0.01)had significantly better survival. Finally, we examinedwhether the lack of an effect of race on post-OLT survivalwas dependent on time periods. Multivariable modelsstratifying on transplant centers for patients before andafter 1994 were created. In the first era (before 1994),with adjustments for age, gender, and pretransplant lab-oratory data, a significantly increased risk of mortality wasfound for patients of other races (HR � 1.60, P � 0.01)

in comparison with Caucasians, whereas African race wasnot associated with mortality (HR � 0.99, P � 0.95).The effect of other race became attenuated once the liverdisease diagnosis [HBV and hepatocellular carcinoma(HCC)] was included in the model (HR � 1.39, P �0.04). In the second era (after 1994), neither African race(HR � 0.47, P � 0.14) nor other race (HR � 1.06, P �0.89) was associated with recipient survival.

DiscussionIn this work, we compared the survival of liver trans-

plant recipients among Caucasian, African American, andother races, using data from 4 academic transplant cen-ters. Although there were noticeable differences in base-line characteristics, such as age, gender, and diagnosis,among the 3 groups, we found no relationship betweenrecipient race and survival. This observation held up inour multivariable analyses, which took into account dif-ferences in pre-OLT characteristics. These results are indirect contradiction to a report (Nair et al.17) based on theUNOS data, which indicated that African and Asian raceswere associated with significantly shorter patient and graftsurvival after OLT in comparison with Caucasian recipi-ents. An examination of our Kaplan-Meier curves and

Fig. 1. Patient (A) and graft (B) survival by race.

Fig. 2. Patient survival in nonfulminant (A) and fulminant (B) hepaticfailure by race.


multivariable HRs indicates that the lack of a difference insurvival between Caucasian and African races that we ob-served was not a result of insufficient power, although oursample size of African American patients was indeedsmaller (n � 135) than that of Nair et al. (n � 1042).Furthermore, in a post hoc sample size calculation, oursample size had enough power to detect a difference of10% in survival, which was about the size of the differencein outcome in the UNOS report.

The most immediate difference between the 2 analysesis that the current work is based on patients from select,high-volume academic medical centers, which may be ex-pected to provide better outcomes than the national aver-age.19 For example, data from UNOS have shown thatcenter volume has a significant impact on recipient sur-vival.20 In fact, there is a substantial difference in survivalbetween UNOS patients and ours. The 5-year patientsurvival in our database was 72% for Caucasian recipientsand 69% for African American counterparts, whereasNair et al.17 reported 5-year survival of 58% for theformer and 48% for the latter. Thus, our patients experi-enced substantially better survival than the national aver-age.

There were intriguing differences in the baseline char-acteristics between Caucasian and African recipients. Af-rican American patients were more likely to havefulminant liver disease, and this was also the case in theUNOS data. Among nonfulminant patients, AfricanAmerican recipients presented with higher MELD labs atthe time of the initial evaluation, although they wereyounger than the patients of other racial groups. This may

suggest that African American patients were referred totransplant centers late in the course of their disease pro-gression. The relative abundance of fulminant diseaseamong African Americans may in fact be due to fewernonfulminant patients being referred to transplant cen-ters. We are not aware of any evidence that African race isassociated with higher susceptibility to acute, fulminantliver disease. In our data, fulminant disease was not asso-ciated with poorer survival in comparison with nonfulmi-nant disease.

Of the potential mechanisms by which a recipient’srace may affect the outcome after OLT, some may have abiological basis. These may include increased tissue in-compatibility between donors and recipients of differentracial backgrounds12 and genetic differences in the metab-olism or effectiveness of immunosuppressant agents.13

Our data suggest that these biological factors are not likelyto account for outcome differences. In the best circum-stances (that is, selected academic centers), African Amer-ican patients did just as well as recipients of other races.

Alternatively, race may be a surrogate for socioeco-nomic factors, such as barriers in access to healthcare orinsurance coverage, socioeconomic status affecting the af-fordability of post-OLT care, and cultural beliefs thatmay affect the acceptance of organ transplantation orposttransplant care.14 An earlier report from the UnitedKingdom suggested that the higher incidence of chronicrejection observed among non-Caucasian recipientscould not be attributed to lower socioeconomic status ornoncompliance.7 A more recent report from the UnitedStates observed that although socioeconomic status hadsome effects on the survival of OLT recipients, race was

Table 3 Univariate Proportional Hazards RegressionAnalysis for Patient Survival**

Factor

HazardRatio (95%Confidence

Interval) P

Race (reference: Caucasian)African 0.90 (0.64,1.26) 0.53Other 1.36 (1.03,1.79) 0.03

Age (decades) 1.25 (1.17,1.34) �0.001Female gender 0.81 (0.70,0.93) 0.004Creatinine* 1.05 (1.01,1.11) 0.03Total bilirubin* 1.01 (1.00,1.01) 0.15Prothrombin time* 1.01 (1.00,1.02) 0.15Diagnosis group

Fulminant hepatic failure (versus not) 1.04 (0.75,1.44) 0.81Cancer (versus not) 1.54 (1.10,2.16) 0.02Alcoholic liver disease (versus not) 1.27 (1.04,1.57) 0.02Viral hepatitis (versus not) 1.57 (1.34,1.83) �0.001Cholestatic disease (versus not) 0.47 (0.38,0.58) �0.001Other (versus not) 0.91 (0.78,1.07) 0.26

* Laboratory data at the time of transplantation.** Analysis stratified on center.

Table 4 Multivariable Proportional Hazards Regression forSurvival Among Patients with Nonfulminant Liver Disease**

Factor

Hazard Ratio (95%Confidence

Interval) P

Race*African 0.85 (0.57, 1.26) 0.42Other 1.25 (0.94, 1.66) 0.13

Age (decades) 1.29 (1.20, 1.39) �0.001Female gender 0.97 (0.83, 1.14) 0.70Total bilirubin† 1.01 (1.003,1.02) 0.01Creatinine† 1.02 (0.95, 1.09) 0.58Prothrombin time† 1.02 (1.00, 1.03) 0.08Diagnosis group‡

Alcoholic liver disease 0.85 (0.67, 1.07) 0.16Cholestatic disease 0.39 (0.30, 0.50) �0.001Cancer 1.23 (0.85, 1.76) 0.27Other 0.68 (0.56, 0.82) �0.001

* Reference: Caucasian.** Analysis stratified on center.† Laboratory data at the time of transplantation.‡ Reference: viral hepatitis.


still an important predictor of survival.18 These studieswere limited because the indicators of socioeconomic sta-tus included only education level, health insurance, orimputed income based on the postal code of the recipi-ent’s residence.21 For our study, one may postulate thatAfrican American patients referred to the centers repre-sented here may be systematically different (for example,higher socioeconomic status) than patients represented inthe UNOS data. Thus, studies conducted so far have notbeen adequate to dissect the complex economic, social,and cultural dynamics that aggregate along racial and eth-nic boundaries.

Our data seem to point to possible barriers for AfricanAmerican patients to liver transplantation: African Amer-ican patients with liver disease may be less likely to bereferred for OLT, unless a young patient is stricken with adramatic illness (that is, fulminant liver disease), or theirreferral may be more likely to be delayed until complica-tions of advanced liver disease develop (that is, highMELD). This interpretation does not necessarily imply abias or discrimination on the part of the provider, as thedelay may be attributed to the payer (or lack thereof) orother socioeconomic circumstances.

It is well established that the pre-OLT recipient statusaffects the post-OLT outcome. On the one hand, AfricanAmerican patients who present with higher levels of sick-ness may be expected to experience poorer outcome afterOLT. On the other hand, the younger age of AfricanAmerican patients may give them an advantage in havinga better outcome. Our multivariable analysis, which in-cluded these pre-OLT predictors, showed that neitherrecipient race nor pre-OLT disease severity had muchimpact on post-OLT survival. Perhaps the impact of thepre-OLT condition on the post-OLT outcome may bemitigated, at least in part, by the experience and resourcesof the transplant center. In contrast, if minority patientshave barriers in access to these centers and are served bycenters less capable of dealing with higher levels of sick-ness prior to OLT, minority race will have an apparentassociation with poor outcome. Thus, we postulate thatthe difference between our data and those of others stemsfrom unequal access to high-quality OLT centers betweenraces. This, however, remains a hypothesis that may betested in the future: the standard UNOS data files madeavailable to researchers do not include center information.Ultimately, to disentangle this and other complex issuesinvolving race and transplant outcome, a focused investi-gation is necessary to address issues such as patient pref-erence, referral patterns for OLT in different race groups,and biases, if any, in the healthcare system with respect toreferring and evaluating minority patients for OLT.

One brief comment may be made about previous ob-servations that Asian race may also be associated with poorpatient survival. A likely explanation for this observationis that there have been more Asian patients with HBVinfection and HCC than Caucasian or African patients.For example, the analysis by Nair et al.17 was based ondata from 1988-1996, when modern methods for pro-phylaxis against HBV recurrence were not available and ahigh incidence of reinfection with HBV and recurrenthepatitis led to graft and patient loss.22-24 In addition, thedata preceded the establishment of criteria for OLT inpatients with HCC, and this may have led to a higherincidence of recurrent HCC and reduced survival inAsian patients in comparison with others.25 The compar-ison of pre-1994 and post-1994 data in our analysis fur-ther corroborates accumulating literature that post-OLTsurvival in recent Asian recipients is comparable to that inrecipients of other racial categories.26-28

As a proof of principle, our data, although put togetherfrom different databases from different time periods, in-dicate that OLT recipients of a minority race, especiallythe African race, should not necessarily be expected tohave poorer survival than Caucasians. Although recipientrace in and of itself may not be a direct predictor of pooroutcome after liver transplantation, socioeconomic fac-tors that correlate with minority race may explain previ-ous observations that have shown such an association.Focused investigations to understand and eliminate bar-riers along socioeconomic and racial boundaries are war-ranted.

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Survival after liver transplantation: Is racial disparity inevitable?