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Hepatitis C, Acute Humoral Rejection, and Renal Allograft Survival

John P. Forman^*,,, Nina Tolkoff-Rubin^,, Manuel Pascual and Julie Lin^*,

*Renal Division, Department of Medicine, Brigham and Women’s Hospital, Renal Unit, Department of Medicine, Massachusetts General Hospital, and Harvard Medical School, Boston, Massachusetts; and Transplant Center, CHUV and Faculty of Medicine, Lausanne, Switzerland.

Correspondence to Dr. Julie Lin, Brigham and Women’s Hospital/Renal Division, 75 Francis Street, MRB-4, Boston, MA 02115. Phone: 617-732-6432; Fax: 617-975-0840; E-mail: jlin11{at}partners.org

	Abstract

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The effect of recipient hepatitis C virus (HCV) infection on renal allograft loss and acute rejection in kidney transplantation remains controversial. We studied 354 renal allograft recipients transplanted during 1996 to 2001 who had HCV antibodies (Ab) measured before transplantation. The primary outcome was death-censored allograft loss and the secondary outcome was acute humoral rejection (AHR). Compared with HCV Ab-negative patients, those with positive HCV Ab had longer time on dialysis before transplantation, higher percentage of panel-reactive antibodies (PRA), were more likely to receive a cadaveric transplant, and were more likely to develop delayed graft function (DGF). In univariate analyses, predictors of renal allograft loss included HCV, cadaveric graft, PRA >20%, HLA mismatch 5, retransplantation, DGF, induction therapy, and AHR. When adjusted for PRA >20%, HLA mismatch 5, and multiple transplant status, HCV was not a statistically significant predictor of allograft loss. HCV was also associated with AHR but lost significance when adjusted for PRA >20%. HCV Ab-positive patients were more likely to have longer duration of dialysis before transplantation prior to kidney transplants, higher PRA, and to receive cadaveric transplants. These characteristics likely resulted in more DGF and AHR after transplantation. After adjusting for these confounding factors, the association between HCV Ab positivity and renal allograft loss was notably attenuated and no longer statistically significant.

	Introduction

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Considerable controversy persists regarding the effect of hepatitis C virus (HCV) on the outcomes of kidney transplantation (1,2). Numerous studies have reported a deleterious effect, with higher rates of acute rejection and allograft loss (3–9). In contrast, an equal number of studies report outcomes that are comparable to those seen in recipients who are not infected with HCV (10–14).

In this study, we examined the effect of HCV Ab status on death-censored allograft survival and acute rejection in kidney transplant recipients. Given the recent advances in the diagnosis of acute humoral rejection (AHR) with specific pathologic criteria outlined by Racusen and others (15) in 1999, and our own interest in this field (16–18), we also specifically asked whether HCV imposed an increased risk of antibody-mediated rejection. Notably, in 1996, Cosio et al. (19) reported that "acute vascular rejection" (possibly due to anti-donor antibodies) was more common in HCV-positive recipients, but this has not been studied in recent years.

	Materials and Methods

Top Abstract Introduction Materials and Methods Results Discussion References

 
Study Design
We performed a retrospective study of 361 patients who received a kidney transplant between January 1, 1996, and December 31, 2001, at Massachusetts General Hospital, where the study was performed. The study cohort was restricted to 354 subjects who had HCV Ab measured before transplantation. This study was approved by the Massachusetts General Hospital Institutional Review Board.

Data Collection
Demographic and clinical data were extracted from review of the medical records. Serum creatinine measures were taken at 1, 3, 6, and 12 mo. After 12 mo, the creatinine was recorded if the test was performed within 3 mo of a predetermined time point of 24, 36, 48, 60, and 72 mo or at end of the study period. Follow-up continued until allograft loss, patient death, or end of the study period on December 31, 2002.

Transplant Operation and Patient Management
The individual surgeons and nephrologists caring for the patients directed perioperative and long-term management. Decisions regarding specific immunosuppression were generally at the discretion of the treating physicians. Beginning in 1997, the majority of patients (85%) were treated with triple immunosuppression consisting of a calcineurin inhibitor, corticosteroids, and mycophenolate mofetil. Before 1997, azathioprine was used rather than mycophenolate mofetil; 42 transplants (11%) were performed before 1997. Sirolimus therapy was used in only 3% of recipients. Antibody induction therapy was generally given if the recipient had an elevated panel-reactive antibody (PRA) (>20%), was undergoing retransplantation, or developed delayed graft function (DGF). Beginning in 2000, recipients of cadaveric transplants received induction therapy. MGH immunosuppressive protocols have been previously described (20).

Definitions
DGF was defined as the transient requirement for dialysis beginning in the first week after the transplant operation. Acute rejection was verified by biopsy in all cases, and classified as acute cellular rejection (ACR), or AHR. ACR was defined according to the Banff criteria (15). AHR was defined histologically by the presence of neutrophils in the glomerular capillaries, and by C4d deposition in the peritubular capillaries (21). C4d staining was standard for all allograft biopsies performed to assess rejection during the study period. Allograft loss was defined as the resumption of chronic dialysis. No subject received preemptive retransplantation. Patients who died with a functioning allograft were censored.

Measurement of Exposure
Hepatitis C antibodies were assessed in 354 out of 361 patients before transplantation as part of the standard workup. Testing was done in the clinical laboratory at Massachusetts General Hospital by means of a commercially available qualitative ELISA assay from Abbot Diagnostics (Abbot Park, IL; sensitivity 72.7%, specificity 99.8%). Testing for HCV RNA was performed by reverse transcriptase PCR (RT-PCR) with the Amplicor HCV Monitor Test obtained from Roche Molecular Diagnostics (Pleasanton, CA). Before 2001, the Massachusetts General Hospital sent samples for RT-PCR to American Medical Laboratories (Chevy Chase, MD).

Outcomes
The primary end point was death censored allograft loss. The secondary end point was the development of AHR.

Statistical Analyses
Fisher’s exact or ² and Wilcoxon rank-sum tests were used to compare categorical and continuous data as appropriate. P 0.05 was considered statistically significant. The primary outcome was analyzed by Kaplan-Meier survival, and multivariable analysis was performed by Cox proportional-hazard regression. The selection of covariates for multivariable models was accomplished by examining proportional-hazard models with (1) individual covariates (univariate proportional hazard), and (2) the outcome of death-censored allograft loss in models with two independent variables (i.e., HCV Ab status and one other covariate). Each covariate was placed in a two-variable model with HCV Ab. Those covariates that changed the hazards for HCV status by >10% were then considered for entry into a multivariable model. For the full multivariable models, we considered covariates that had a statistically significant association with HCV Ab-positive status (the exposure of interest) and the primary outcome of death-censored allograft loss. We also limited the number of exposure variables to a maximum of four to minimize overfitting of data, keeping to the rule of thumb that there should be no more than one variable for every ten events, as there were 31 death-censored graft losses in our data set. Because the time at which AHR occurs after transplantation is variable, we treated AHR as a time-varying covariate in all proportional-hazard models.

For the secondary outcome of AHR, we noted that 68% of the events occurred within the first month after transplantation. We then formally tested the proportional-hazard assumption by introducing a time-varying covariate into a model with AHR as the dependent variable and HCV status as the independent variable and found a significant interaction between time and HCV status (P = 0.03)—that is, the proportional-hazard assumption of constant hazard over time therefore did not hold. We also plotted the hazard functions for AHR by HCV status and confirmed that the hazards crossed several times. Consequently, we decided to perform logistic regression for testing associations with AHR.

	Results

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Three hundred sixty-one kidney transplants were performed from January 1996 through December 2001. ESRD was attributed to glomerulonephritis (including focal sclerosis) in 35.2% of subjects. Other causes of ESRD included diabetes (21.3%), polycystic kidney disease (10.5%), obstruction or reflux (7.8%), hypertension (5.8%), and hereditary nephritis (4.4%). Pretransplant HCV Ab was measured in 354 patients. Twenty-six (7.3%) were positive for antibodies to HCV, and HCV RNA quantitative titers measured in 13 patients ranged from zero to 1,264,667 copies/ml; one patient with an HCV Ab titer that was positive on two separate occasions had a negative virus load. The median length of follow-up was 28 mo.

Baseline characteristics before transplantation stratified by HCV Ab status are given in Table 1. Patients with and without pretransplant HCV Ab did not differ with respect to age, gender, diabetes, hypertension, or number of HLA mismatches. Patients positive for HCV Ab spent longer amounts of time on dialysis before transplantation (41 versus 23 mo, P = 0.009), were more sensitized (31% versus 12% had PRA >20%, P = 0.01) and were more likely to be receiving their second or third transplant 42% versus 9%, P < 0.0001). Also, HCV Ab-positive patients were more likely to receive a cadaveric kidney (77% versus 47%, P = 0.01).

Events after transplantation are shown in Table 2. Patients with and without positive HCV Ab titers were similar in terms of the development of ACR, but HCV Ab-positive patients had more AHR (19% versus 6%, P = 0.02), more DGF (25% versus 12.3%, P = 0.05), and had higher 1-mo serum creatinine concentrations after transplantation (1.9 mg/dl versus 1.5 mg/dl, P = 0.003). Serum creatinine was no longer significantly different after 12 mo of follow-up (1.5 mg/dl versus 1.6 mg/dl, P = 0.47). Ten subjects died with functioning allografts during the study period, two of whom were HCV Ab positive. In the HCV-positive group, the cause of death was sepsis in one of these patients and colorectal cancer in the other. Death with a functioning allograft in HCV-negative patients resulted from stroke (two subjects), pulmonary embolism (two subjects), posttransplant lymphoproliferative disease (two subjects), arrhythmia (one subject), and lung cancer (one subject).

View larger version (16K): [in this window] [in a new window] [as a PowerPoint slide]   Figure 1. Kaplan-Meier plot of death-censored allograft survival stratified by hepatitis C virus antibody status.

Because a previous report suggested a link between AHR and treatment of HCV Ab-positive recipients with IFN- after transplantation (18), we analyzed the 26 recipients in our population with HCV for an association between posttransplant IFN- administration and humoral rejection. Nine (35%) of 26 patients were treated with IFN-. Among those not treated, three (18%) developed humoral rejection, whereas two (22%) of those treated with IFN- developed humoral rejection (P = 1.0). We found no association between IFN- therapy for HCV and the development of AHR.

We also examined the effect of coexisting HCV and anticardiolipin antibodies because a previous report found an association between renal transplant microangiopathy and coexistence of these antibodies (22). Five of the HCV Ab-positive patients also had positive anticardiolipin antibody titers, although none of them had the antiphospholipid syndrome before transplantation. We did not observe differences in the primary outcome between HCV Ab-positive patients with or without anticardiolipin antibodies. Furthermore, three of these five recipients underwent allograft biopsies, and no thrombotic microangiopathy was noted.

When a sensitivity analysis was performed with the composite end point of allograft loss or death with a functioning allograft, the HR for HCV status in the multivariable model did not change (HR = 3.26; 95% CI, 1.50 to 7.08). Multivariable modeling with the composite end point only changed the HR for HCV status by <10% in all models (data not shown).

	Discussion

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We conducted a retrospective observational cohort study to determine whether pretransplant HCV antibody status is an independent risk factor for renal allograft loss after kidney transplantation. Our study population was similar to others reported in the literature, with HCV Ab-positive patients having a longer time on dialysis, higher sensitization, greater frequency of retransplantation, and more cadaveric donation (3–5). These risk factors have been reported to be associated with the development of AHR and DGF (17). After adjusting for confounding by pretransplant or posttransplant variables, HCV Ab positivity was associated with a HR of 1.7 to 2.0 for allograft loss, but was no longer statistically significant because the 95% CI included one.

Our results are consistent with the findings of several previously published reports. Periera et al. (5) found no overall difference in graft survival with 45 mo of follow-up. In other cohorts, investigators have also found equivalent rates of graft loss in HCV Ab-positive patients compared with Ab-negative patients (6,10,11). In the largest analysis to date, Meier-Kriesche et al.(3) examined data on over 73,000 transplant recipients using the United States Renal Data System. Although they found no significant difference in death censored renal allograft loss with 8 yr of follow-up, they noted a trend toward worse graft survival, with approximately 70% of grafts surviving at 5 yr compared with approximately 80% in those with negative HCV Ab titers.

In contrast, several investigators have reported significantly higher rates of renal allograft loss in HCV Ab positive patients. Legendre et al. (7) found a 25% relative reduction in graft survival at 12 yr, and Gonzalez-Roncero et al. (8) reported a significant 15% reduced graft survival at 1 yr. Gentil et al. (4) found a threefold increase in relative risk of renal allograft loss at 5 yr.

It should be noted that among these reports, only the study by Gentil et al. (4) used multivariable analysis to examine the independent effect of HCV Ab status on renal allograft outcomes. Because recipient hepatitis C Ab positivity has repeatedly been shown to correlate with higher PRA, high rates of retransplantation, and cadaveric donation, adjustment for potential confounding by these factors needs to be performed. The Gentil study examined cadaveric recipients only, and adjusted for multiple pretransplant covariates. They also found significantly higher PRA (a PRA>50% was present in 10.7% of HCV Ab positive patients versus 1.3% of HCV-negative patients, P = 0.001) and higher retransplantation rates (10.6% versus 4.3%, P = 0.034) in hepatitis C positive patients, but these variables were excluded from their multivariable analysis because they barely missed reaching statistical significance as predictors of graft loss in univariate analysis with reported p-values ranging from 0.056 to 0.12). Of note, however, several studies have reported PRA to be an important predictor of renal graft loss (22–24). We also found higher PRA and retransplantation to be predictive of renal allograft loss in univariate analysis. Therefore, we feel that our study and the Gentil study are not absolutely contradictory because differences in the choice of predictors to include in the final multivariable model could account for the dissimilar statistical results.

We also observed that patients with positive hepatitis C serology had higher rates of AHR, a result not previously reported. This association barely lost statistical significance after adjustment for higher PRA (HR = 3.06; 95% CI, 0.99 to 9.39), which is a previously described risk factor for AHR (17). Interestingly, Cosio et al. (19) described "acute vascular rejection" in 60% of HCV positive recipients compared with 28% in those without HCV who underwent renal allograft biopsy. It is possible that the authors were detecting antibody-mediated rejection, but because specific pathologic criteria were not described in that report, this is difficult to ascertain.

We found no association between hepatitis C serology and ACR. It should be noted that studies examining the effect of HCV on rejection have not distinguished between humoral and cellular rejection. The results of previously published reports have varied from decreased rejection rates in HCV-positive patients (5,12), equivalent rejection rates (4,13,14,25,26), and higher rejection rates in HCV-positive patients (3,6).

A possible link between HCV and AHR was recently reported by our group in a case series by Baid et al. (18) using a subset of HCV positive patients who received IFN- therapy. In that report, 12 patients with HCV received IFN- after transplantation, and 2 (17%) developed AHR within 6 mo of initiating therapy. Until now, no further study had investigated the rates of humoral rejection in HCV positive renal transplant recipients, or whether an association exists between humoral rejection and IFN- therapy. One of the two patients who had AHR in the setting of IFN- therapy from the previously published series was also included in our analysis. Although the rate of AHR in recipients treated with IFN- was generally high in our study (22%), it was not different from the rate of AHR in HCV-positive patients without IFN- treatment (24%). Also, the association of HCV Ab-positivity and AHR appears to be confounded by the presence of high sensitization.

The results of our analysis must be interpreted in the context of the study design. The number of patients reaching the primary end point of allograft loss was relatively small (n = 31) because of excellent transplant outcomes in general. Therefore, it is possible that there may be a type 2 error (false-negative finding) because of low power. This is also applicable to the potential relationship between HCV and AHR, as the effect estimate is high and the lower confidence bound barely included the null value (HR = 3.06; 95% CI, 0.99 to 9.39).

The median follow-up of this study was between 2 and 3 yr. It is conceivable that HCV may have a deleterious effect on graft survival only after a much longer period of follow-up after transplantation, as Legendre et al. (7) showed in their univariate analysis; however, other unadjusted analyses with long-term follow-up have found no relationship between HCV Ab status and graft loss (3,11).

Because our study relied upon medical record review, there was a potential for misclassification. But because the outcomes in this study of allograft loss and biopsy proven acute rejection are well defined, misclassification is unlikely. The exposure of interest, HCV Ab positivity, was confirmed in 12 of 26 patients by a quantitative virus load whereas previously published studies did not report verification of chronic hepatitis C infection. It is possible that loss to follow-up could be a potential source of bias, but there was no difference in duration of follow-up. Despite these limitations, this and the study by Gentil et al. (4) are the only investigations that performed multivariable analyses of the relation between HCV Ab status and death censored allograft loss in a renal transplant cohort. This is also the first report of an association between HCV and AHR, which may be attributable in part to the higher pretransplant PRA levels in those with positive HCV titers.

In summary, we identified an increased risk of renal allograft loss in HCV Ab-positive recipients but also observed strong associations between this pretransplant exposure and longer duration of dialysis, higher PRA, retransplantation, and a higher frequency of cadaveric grafts. These factors are known to be associated with higher rates of DGF and AHR; with adjustment for these confounders, the association of HCV Ab positivity with renal allograft loss was markedly attenuated in several multivariable models. With the exception of one investigation (4), previous reports of an association between hepatitis C and increased renal allograft loss did not adjust for potential confounders. Therefore, we propose that HCV Ab positivity may not be an independent risk factor for renal allograft loss at approximately 3 yr after kidney transplantation.

	Acknowledgments

 
Part of this work was presented as a poster at the 2003 American Society of Nephrology Meeting in San Diego, CA. Dr. Manuel Pascual is supported by the LEENAARDS Foundation. Dr. Julie Lin is supported by NIH grant K08 DK066246 from the NIDDK.

	References

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Forman, J. P. Articles by Lin, J. Search for Related Content PubMed PubMed Citation Articles by Forman, J. P. Articles by Lin, J.