Abstract
Summary
Background and objectives
Hepatitis C virus (HCV) infection is associated with increased mortality and morbidity in end-stage renal failure (ESRF) patients. Despite a lower incidence and risk of transmission of HCV infection with peritoneal dialysis (PD), the optimal dialysis modality for HCV-infected ESRF patients is not known. The aim of this study was to evaluate the impact of dialysis modality on the survival of HCV-infected ESRF patients.
Design, setting, participants, & measurements
The study included all adult incident ESRF patients in Australia and New Zealand who commenced dialysis between January 1, 1994, and December 31, 2008, and were HCV antibody-positive at the time of dialysis commencement. Time to all-cause mortality was compared between hemodialysis (HD) and PD according to modality assignment at day 90, using Cox proportional hazards model analysis.
Results
A total of 424 HCV-infected ESRF patients commenced dialysis during the study period and survived for at least 90 days (PD n = 134; HD n = 290). Mortality rates were comparable between PD and HD in the first year (10.7 versus 13.8 deaths per 100 patient-years, respectively; adjusted hazard ratio [HR] 0.65, 95% CI 0.34 to 1.26) and thereafter (20 versus 15.9 deaths per 100 patient-years, respectively; HR 1.27, 95% CI 0.86 to 1.88).
Conclusions
The survival of HCV-infected ESRF patients is comparable between PD and HD.
Introduction
Chronic hepatitis C virus (HCV) infection is an important problem in end-stage renal failure (ESRF) patients receiving maintenance dialysis, with reported prevalence rates ranging between 0.7% and 76% in different countries around the world (1–4). The presence of HCV antibody has been shown to be a significant risk factor for morbidity and mortality in dialysis populations (2,5–8), possibly due to HCV-associated hepatic cirrhosis, hepatocellular carcinoma, and cardiovascular disease (5,6).
The incidence and prevalence of HCV infection are significantly lower in patients receiving peritoneal dialysis (PD) compared with those receiving hemodialysis (HD) (2,9–15). The postulated reasons for this observation include reduced blood transfusion requirements in PD patients (3,15–17) and the more isolated practice of dialysis at home with minimized visits to the renal unit (every 1 to 3 months for PD rather than thrice weekly for HD) (2). Furthermore, a number of studies suggest that environmental transmission within dialysis units is a major risk factor for HCV transmission in HD patients (4,14,15). PD may therefore be an attractive option for ESRF patients with HCV infection to minimize transmission to other patients, provided survival was at least comparable to that of HD.
Unfortunately, the impact of dialysis modality on the survival of HCV-infected patients with ESRF has been subject to limited investigation. A recent publication by Chou et al. (18) of 78 PD patients and 78 propensity score-matched HD patients with chronic HCV infection reported similar survival rates. However, this study was limited by small sample size, insufficient statistical power, and single-center design. The aim of the present multicenter and multicountry investigation was to evaluate the impact of dialysis modality on the survival of HCV antibody-positive patients with ESRF.
Materials and Methods
Study Population
This retrospective, observational cohort study included all adult ESRF patients in Australia and New Zealand who were older than 18 years, commenced dialysis between January 1, 1994, and December 31, 2008, and were HCV antibody-positive at the time of dialysis commencement. HCV testing is uniformly performed on patients treated with dialysis in Australia and New Zealand, and the results of these tests are reported to the Australian and New Zealand Dialysis and Transplant (ANZDATA) Registry. Recipients of pre-emptive kidney transplants and those who died or were transplanted in the first 90 days of dialysis commencement were excluded. Follow-up continued until December 31, 2008. Dialysis modality was assigned according to whether patients were receiving PD or HD on day 90 after renal replacement therapy commencement. Other data collected included demographic data, cause of primary renal disease, comorbidities at the start of dialysis (coronary artery disease, peripheral vascular disease, cerebrovascular disease, chronic lung disease, diabetes, hypertension, and smoking status), body mass index, and late referral (defined as commencement of dialysis within 3 months of referral to a nephrologist). The primary outcome measure was survival.
Statistical Analyses
Results were expressed as frequencies and percentages for categorical variables, mean ± SD for continuous normally distributed variables, and median and interquartile range for continuous non-normally distributed variables. Baseline analyses were carried out by dividing patients into two groups according to whether they were receiving PD or HD at day 90. Differences between the two groups were analyzed by the chi-squared test for categorical data, the unpaired t test for continuous normally distributed data, and the Mann-Whitney test for continuous non-normally distributed data. Survival curves, survival probabilities, and estimated mean survival times were generated according to the Kaplan-Meier method on an intention-to-treat basis according to dialysis modality at 90 days. Differences in the survival curves between the two groups were evaluated using the log rank test. Time to death was also evaluated by multivariate Cox proportional hazards survival analysis with backward stepwise elimination to identify the most parsimonious model. The covariates initially included in the model were age, gender, racial origin, body mass index, late referral (referral to nephrologist within 3 months of commencing renal replacement therapy), smoking status (never, former, or current), chronic lung disease, coronary artery disease, cerebrovascular disease, peripheral vascular disease, diabetes mellitus, and dialysis era. Complete data were available on all covariates. Data were censored for renal transplantation, recovery of renal function, loss to follow-up, and end of study (December 31, 2008). Proportional hazards assumptions were checked by Schoenfeld residuals and scaled Schoenfeld residuals, examined by formal hypothesis test and graphically. First-order interaction terms between the significant covariates were examined for all models. There was no evidence of an interaction between modality and dialysis era. Data were analyzed using Stata/IC 10 (College Station, TX). P-values <0.05 were considered statistically significant.
Results
A total of 424 HCV antibody-positive, ESRF patients commenced dialysis in Australia and New Zealand during the study period (January 1, 1994, to December 31, 2008) and survived for at least 90 days. On day 90 after dialysis commencement, 134 (32%) patients were receiving PD and 290 (69%) were receiving HD. The baseline characteristics of the two groups were comparable, although there was a trend toward more frequent occurrence of female gender and coronary artery disease in the PD group (Table 1). The proportion of HCV-infected ESRF patients treated with PD at day 90 (32%) was slightly lower than that reported for the general ESRF population in Australia and New Zealand (42%) (19). Of the 290 HD patients, 287 (99%) were receiving facility-based HD. The rates of transplantation were comparable between HD and PD (5-year cumulative rate 17% versus 14%).
Table 1.
Characteristics of all 424 HCV antibody-positive, ESRF patients receiving hemodialysis or peritoneal dialysis in Australia and New Zealand during the period 1994 to 2008
| Characteristic | HD (n = 290)a | PD (n = 134)a | P |
|---|---|---|---|
| Age (years)b | 57.8 ± 17.0 | 57.4 ± 17.8 | 0.40 |
| Women | 84 (29) | 49 (37) | 0.12 |
| Racial origin | 0.18 | ||
| nonindigenous | 250 (86) | 122 (91) | |
| Aboriginal/Torres Strait Islander | 22 (8) | 4 (3) | |
| Maori/Pacific Islander | 18 (6) | 8 (6) | |
| Body mass indexc | 0.24 | ||
| underweight (<20) | 28 (10) | 18 (13) | |
| normal (20 to 24.9) | 114 (39) | 58 (43) | |
| overweight (25 to 29.9) | 85 (29) | 39 (29) | |
| obese (≥30) | 63 (22) | 19 (14) | |
| late referral | 90 (31) | 42 (31) | 0.95 |
| ESRF cause | 0.26 | ||
| chronic glomerulonephritis | 93 (32) | 37 (28) | |
| diabetic nephropathy | 98 (34) | 59 (44) | |
| renovascular disease | 27 (9) | 7 (5) | |
| polycystic kidneys | 11 (4) | 1 (1) | |
| reflux nephropathy | 13 (4) | 5 (4) | |
| analgesic nephropathy | 7 (2) | 4 (3) | |
| other | 22 (8) | 13 (10) | |
| unknown | 19 (7) | 8 (6) | |
| Current smoking | 103 (36) | 51 (38) | 0.61 |
| Chronic lung disease | 45 (15) | 21 (16) | 0.97 |
| Coronary artery disease | 82 (28) | 49 (37) | 0.09 |
| Peripheral vascular disease | 67 (23) | 39 (29) | 0.19 |
| Cerebrovascular disease | 27 (9) | 17 (13) | 0.29 |
| Diabetes mellitus | 0.17 | ||
| no | 159 (55) | 63 (47) | |
| type 1 | 26 (9) | 19 (14) | |
| type 2 | 105 (36) | 52 (39) | |
| Hypertension | 197 (68) | 97 (72) | 0.36 |
| Dialysis era | 0.53 | ||
| 1994 to 1995 | 16 (5) | 7 (5) | |
| 1996 to 1997 | 25 (9) | 17 (13) | |
| 1998 to 1999 | 38 (13) | 17 (13) | |
| 2000 to 2001 | 30 (10) | 20 (15) | |
| 2002 to 2003 | 49 (17) | 20 (15) | |
| 2004 to 2005 | 56 (19) | 21 (16) | |
| 2006 to 2007 | 52 (18) | 26 (19) | |
| 2008 | 24 (8) | 6 (5) |
HCV, hepatitis C virus; ESRF, end-stage renal failure; HD, hemodialysis; PD, peritoneal dialysis.
Values are number of subjects with percentage in parentheses.
Values are expressed as mean ± SD.
Calculated as weight in kilograms divided by height in meters squared (kg/m2).
One hundred ninety-nine (47%) HCV antibody-positive patients died during the study; 37 (19%) died in the first year of dialysis commencement, and 162 (81%) died after the first year. Overall, 128 (44%) died in the HD group (27 in the first year and 101 thereafter), and 71 (53%) died in the PD group (10 in the first year and 61 thereafter) (P = 0.37). The main causes of death in the HD and PD groups were cardiovascular (49% versus 43%) and infectious (8% versus 23%). On Kaplan-Meier analysis, there was no significant difference in survival between the two groups (log rank statistic 0.82, P = 0.37, Figure 1).
Figure 1.
Kaplan-Meier survival curve for 424 hepatitis C virus antibody-positive end-stage renal failure patients treated with hemodialysis (n = 290) or peritoneal dialysis (n = 134) in Australia and New Zealand during the period 1994 to 1998. HD, hemodialysis; PD, peritoneal dialysis.
To deal with potential nonproportional hazards, the follow-up period was divided into survival over the first year of dialysis and after 1 year of dialysis. Using Cox regression analysis, the mortality rates in the first year of dialysis were 13.8 per 100 patient-years (95% CI 9.46 to 20.1) in the HD group and 10.7 per 100 patient years (95% CI 5.7 to 19.8) in the PD group (univariate hazard ratio [HR] PD versus HD 0.78, 95% CI 0.42 to 1.43). After the first year of dialysis, the mortality rates were 15.9 per 100 patient-years (95% CI 13.1 to 19.4) in the HD group and 20.0 per 100 patient years (95% CI 15.5 to 25.7) in the PD group (univariate HR PD versus HD 1.24, 95% CI 0.85 to 1.80). After adjusting for other baseline characteristics in a multivariate Cox proportional hazards model using backward stepwise elimination to identify the most parsimonious model, there was no significant difference in the mortality of HCV antibody-positive patients according to whether they received PD or HD on day 90 (first year of dialysis adjusted HR 0.65, 95% CI 0.34 to 1.26; subsequent years of dialysis HR 1.27, 95% CI 0.86 to 1.88) (Table 2). Similar results were observed using an as-treated analysis (first year of dialysis adjusted HR 0.63, 95% CI 0.36 to 1.13; subsequent years of dialysis HR 1.08, 95% CI 0.72 to 1.62).
Table 2.
Results of multivariate Cox proportional hazards model analysis of time to death in 424 HCV antibody-positive ESRF patients treated with hemodialysis (n = 290) or peritoneal dialysis (n = 134) in Australia and New Zealand during the period 1994 to 1998
| Variable | HRa | P |
|---|---|---|
| PD (first year of dialysis)b | 0.65 (0.34 to 1.26) | 0.20 |
| PD (after first year of dialysis)b | 1.27 (0.86 to 1.88) | 0.24 |
| Age (per year) | 1.03 (1.01 to 1.04) | <0.01 |
| Male gender | 0.73 (0.56 to 0.97) | 0.03 |
| ESRF cause | ||
| chronic glomerulonephritis | Reference | — |
| diabetic nephropathy | 1.41 (0.59 to 3.39) | 0.44 |
| renovascular disease | 1.83 (0.92 to 3.63) | 0.08 |
| polycystic kidneys | 1.49 (0.75 to 2.95) | 0.25 |
| reflux nephropathy | 0.97 (0.39 to 2.41) | 0.95 |
| analgaesic nephropathy | 1.50 (0.74 to 3.07) | 0.26 |
| other | 2.31 (1.34 to 3.98) | <0.01 |
| unknown | 1.98 (1.09 to 3.61) | 0.02 |
| Smoking status | ||
| current | Reference | — |
| former | 0.84 (0.60 to 1.18) | 0.32 |
| never | 0.70 (0.50 to 0.97) | 0.03 |
| Coronary artery disease | 1.75 (1.34 to 2.30) | <0.01 |
| Peripheral vascular disease | 1.40 (1.04 to 1.89) | 0.03 |
| Diabetes mellitus | ||
| no | Reference | — |
| type 1 | 2.22 (1.03 to 4.79) | 0.04 |
| type 2 | 1.21 (0.70 to 2.09) | 0.50 |
HCV, hepatitis C virus; HR, hazard ratio; PD, peritoneal dialysis; HD, hemodialysis; ESRF, end-stage renal failure; —, not applicable.
Values in parentheses are 95% confidence intervals.
Due to nonproportional hazards for death observed with dialysis modality over time, the HRs for PD (relative to HD) are presented separately for the first year of dialysis and for subsequent years of dialysis. Backward stepwise elimination was used to identify the most parsimonious model.
In view of the small number of deaths in the first year (particularly in the PD group), which may have affected statistical power and the stability of estimates, further intention-to-treat analyses were performed using the 90 days dialysis modality as a time-varying covariate in linear, log, and exponential decay models, rather than using two time-varying categories (≤ or >1 year of dialysis). In these models, the hazard ratios for PD relative to HD were 1.05 (95% CI 0.71 to 1.57), 1.03 (95% CI 0.73 to 1.47), and 1.24 (95% CI 0.77 to 2.02), respectively. Moreover, the time varying term did not reach statistical significance in either the linear (P = 0.68), log (P = 0.49), or exponential decay models (P = 0.41), indicating that the variation in hazard by dialysis modality over time was not statistically significant.
Discussion
The present study is the largest and only comprehensive multicenter investigation to date of the impact of dialysis modality on the survival of HCV antibody-positive patients with ESRF. All-cause mortality rates were comparable between HD and PD on both univariate and multivariate analysis.
Our findings are in keeping with those of a previous, small, retrospective, case-control analysis from Taiwan (18), in which the survival of 78 PD patients with chronic HCV infection was observed to be comparable to that of 78 propensity score-matched HD patients with chronic HCV infection (univariate hazard ratio PD versus HD 1.24, 95% CI 0.78 to 1.99). These results were remarkably similar to those of the present investigation, in spite of the higher mortality rates in the former study (median survival for HCV-infected PD patients 2.2 versus 4.5 years, respectively) and the 10-fold higher HCV prevalence rates in Taiwanese compared with Australasian ESRF patient populations (2,18). On forward stepwise Cox regression, Chou et al. (18) found that the significant independent predictors of mortality in HCV-infected ESRF patients were positivity for hepatitis B virus surface antigen (P < 0.01), diabetes mellitus (P = 0.01), and serum albumin (P = 0.03). In contrast, the major risk factors for death in our study were older age, female gender, ESRF cause, smoking, coronary artery disease, and dialysis era. Diabetes mellitus was not independently associated with mortality, and serum albumin and hepatitis B virus surface antigen status were not collected.
Taken together, these results suggest that survival rates of HCV-infected patients on PD and HD are comparable and that outcome considerations should not generally impact on decisions regarding dialysis modality selection for HCV-positive ESRF patients. Although a type 2 statistical error cannot be entirely excluded, it is estimated that the present study had 80% power to detect at least a 28% reduction in mortality of HCV antibody patients treated with PD compared with HD. In light of the negative association between dialysis modality and survival of HCV-infected ESRF patients, PD may be an attractive option for such patients because it is associated with a threefold lower risk of HCV transmission to other dialysis patients compared with HD (2). Interestingly, the point estimates for mortality of HCV-infected patients were lower for PD than HD in the first year and higher thereafter. Although these results did not reach statistical significance, they do mirror the findings reported for the effect of dialysis modality on mortality in general dialysis populations (19–22).
The overall survival of HCV-infected patients on dialysis in this study was inferior to that of the general dialysis population in Australia and New Zealand (19). Our group has previously shown that mortality on dialysis was predicted by either the presence of anti-HCV antibody at baseline (adjusted HR 1.29, 95% CI 1.05 to 1.58, P = 0.02) or the development of anti-HCV antibodies during the course of dialysis (adjusted HR 1.27, 95% CI 1.04 to 1.55, P = 0.02) (2). Similar findings were reported in a meta-analysis of one case-control and three prospective cohort studies of 2314 maintenance dialysis patients (23), in which the presence of anti-HCV antibody was an independent and significant risk factor for death (relative risk 1.57, 95% CI 1.33 to 1.86). Although some of this excess mortality risk can be attributed to hepatic cirrhosis and hepatocellular carcinoma (2,23), the most common cause of death of HCV-infected patients in our study was cardiovascular. Chou et al. (18) reported an identical finding.
The strengths of this study included its very large sample size and inclusiveness. We included all HCV antibody-positive patients receiving dialysis in Australia and New Zealand during the study period, such that a variety of centers were included with varying approaches to HCV and dialysis management. This greatly enhanced the external validity of our findings. These strengths should be balanced against the study's limitations, which included limited depth of data collection. ANZDATA does not collect important information, such as the HCV antibody assay used, laboratory results (such as hepatic transaminase levels, other liver function tests, serum albumin, coagulation profile, HCV RNA titer, liver histology), severity of comorbidities, HCV treatment (including pegylated IFN), and individual unit HCV and dialysis management protocols. Even although we adjusted for a large number of patient characteristics, the possibility of residual confounding could not be excluded. In common with other registries, ANZDATA is a voluntary registry, and there is no external audit of data accuracy, including the diagnosis of chronic HCV infection. Consequently, the possibility of coding/classification bias cannot be excluded.
Conclusions
This study demonstrated that the survival of HCV-infected ESRF patients is comparable between HD and PD, such that outcome considerations should not generally impact on decisions regarding dialysis modality selection for HCV-positive ESRF patients.
Disclosures
Statement of Competing Financial Interests
David Johnson is a consultant for Baxter Healthcare Pty Ltd. and has previously received research funds from this company. He has also received speakers' honoraria and research grants from Fresenius Medical Care and is a recipient of a Queensland Government Health Research Fellowship. Dr. Kym Bannister is a consultant for Baxter Healthcare Pty Ltd. Dr. Fiona Brown is a consultant for Baxter and Fresenius and has received travel grants from Amgen and Roche. Dr. Stephen McDonald has received speaking honoraria from AMGEN Australia, Fresenius Australia, and Solvay Pharmaceuticals and travel grants from AMGEN Australia, Genzyme Australia, and Jansen-Cilag. The remaining authors have no competing financial interests to declare.
Acknowledgments
The authors gratefully acknowledge the substantial contributions of the entire Australia and New Zealand nephrology community (physicians, surgeons, database managers, nurses, renal operators, and patients) in providing information for and maintaining the ANZDATA Registry database.
Footnotes
Published online ahead of print. Publication date available at www.cjasn.org.
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