Kathryn J. Wiggins,* Kym M. Bannister,*¶ Neil Boudville,* ** Philip Clayton,* â â and David W. Johnson*â . Summary. Background and objectives Hepatitis C virus ...
Article
Effect of Dialysis Modality on Survival of Hepatitis C-Infected ESRF Patients Bhadran Bose,*† Stephen P. McDonald,*‡ Carmel M. Hawley,*† Fiona G. Brown,*§ Sunil V. Badve,*† Kathryn J. Wiggins,* Kym M. Bannister,*¶ Neil Boudville,* ** Philip Clayton,* †† and David W. Johnson*†
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. Clin J Am Soc Nephrol 6: 2657–2661, 2011. doi: 10.2215/CJN.02200311
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 www.cjasn.org Vol 6 November, 2011
*Australia and New Zealand Dialysis and Transplant Registry, Adelaide, Australia; † Department of Renal Medicine, University of Queensland at Princess Alexandra Hospital, Brisbane, Australia; ‡ Department of Nephrology and Transplantation Services, University of Adelaide at Central Nothern Adelaide Renal & Transplant Services, Adelaide, Australia; § Department of Nephrology, Monash Medical Center, Clayton, Victoria, Australia; 储University of Melbourne Department of Medicine, St. Vincent’s Hospital, Fitzroy, Victoria, Australia; ¶Department of Nephrology, University of Adelaide at Central Nothern Adelaide Renal & Transplant Services, Adelaide, Australia; **Department of Medicine, University of Western Australia, Perth, Australia; and †† Department of Renal Medicine, Royal Prince Alfred Hospital, Sydney, Australia
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- Correspondence: Dr. David Johnson, positive patients with ESRF. Department of
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 Aus-
Nephrology, Level 2, ARTS Building, Princess Alexandra Hospital, Ipswich Road, Woolloongabba, Brisbane, Qld 4102, Australia; Phone: ⫹61 7 3240 5080; Fax: ⫹61 7 3240 5480; E-mail: david_johnson@health. qld.gov.au
Copyright © 2011 by the American Society of Nephrology
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tralia 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-totreat 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%). 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). 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). 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 timevarying categories (ⱕ 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
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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 Women Racial origin nonindigenous Aboriginal/Torres Strait Islander Maori/Pacific Islander Body mass indexc underweight (⬍20) normal (20 to 24.9) overweight (25 to 29.9) obese (ⱖ30) late referral ESRF cause chronic glomerulonephritis diabetic nephropathy renovascular disease polycystic kidneys reflux nephropathy analgesic nephropathy other unknown Current smoking Chronic lung disease Coronary artery disease Peripheral vascular disease Cerebrovascular disease Diabetes mellitus no type 1 type 2 Hypertension Dialysis era 1994 to 1995 1996 to 1997 1998 to 1999 2000 to 2001 2002 to 2003 2004 to 2005 2006 to 2007 2008
57.8 ⫾ 17.0 84 (29)
57.4 ⫾ 17.8 49 (37)
0.40 0.12 0.18
250 (86) 22 (8) 18 (6)
122 (91) 4 (3) 8 (6)
28 (10) 114 (39) 85 (29) 63 (22) 90 (31)
18 (13) 58 (43) 39 (29) 19 (14) 42 (31)
93 (32) 98 (34) 27 (9) 11 (4) 13 (4) 7 (2) 22 (8) 19 (7) 103 (36) 45 (15) 82 (28) 67 (23) 27 (9)
37 (28) 59 (44) 7 (5) 1 (1) 5 (4) 4 (3) 13 (10) 8 (6) 51 (38) 21 (16) 49 (37) 39 (29) 17 (13)
159 (55) 26 (9) 105 (36) 197 (68)
63 (47) 19 (14) 52 (39) 97 (72)
16 (5) 25 (9) 38 (13) 30 (10) 49 (17) 56 (19) 52 (18) 24 (8)
7 (5) 17 (13) 17 (13) 20 (15) 20 (15) 21 (16) 26 (19) 6 (5)
0.24
0.95 0.26
0.61 0.97 0.09 0.19 0.29 0.17
0.36 0.53
HCV, hepatitis C virus; ESRF, end-stage renal failure; HD, hemodialysis; PD, peritoneal dialysis. a Values are number of subjects with percentage in parentheses. b Values are expressed as mean ⫾ SD. c Calculated as weight in kilograms divided by height in meters squared (kg/m2).
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 mel-
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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 ⴝ 290) or peritoneal dialysis (n ⴝ 134) in Australia and New Zealand during the period 1994 to 1998
Figure 1. | Kaplan-Meier survival curve for 424 hepatitis C virus antibody-positive end-stage renal failure patients treated with hemodialysis (n ⴝ 290) or peritoneal dialysis (n ⴝ 134) in Australia and New Zealand during the period 1994 to 1998. HD, hemodialysis; PD, peritoneal dialysis.
litus (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 HCVinfected 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 carci-
Variable
HRa
PD (first year of dialysis)b PD (after first year of dialysis)b Age (per year) Male gender ESRF cause chronic glomerulonephritis diabetic nephropathy renovascular disease polycystic kidneys reflux nephropathy analgaesic nephropathy other unknown Smoking status current former never Coronary artery disease Peripheral vascular disease Diabetes mellitus no type 1 type 2
0.65 (0.34 to 1.26) 1.27 (0.86 to 1.88)
0.20 0.24
1.03 (1.01 to 1.04) 0.73 (0.56 to 0.97)
⬍0.01 0.03
Reference
—
1.41 (0.59 to 3.39) 1.83 (0.92 to 3.63) 1.49 (0.75 to 2.95) 0.97 (0.39 to 2.41) 1.50 (0.74 to 3.07) 2.31 (1.34 to 3.98) 1.98 (1.09 to 3.61)
0.44 0.08 0.25 0.95 0.26 ⬍0.01 0.02
Reference 0.84 (0.60 to 1.18) 0.70 (0.50 to 0.97) 1.75 (1.34 to 2.30) 1.40 (1.04 to 1.89)
— 0.32 0.03 ⬍0.01 0.03
Reference 2.22 (1.03 to 4.79) 1.21 (0.70 to 2.09)
— 0.04 0.50
P
HCV, hepatitis C virus; HR, hazard ratio; PD, peritoneal dialysis; HD, hemodialysis; ESRF, end-stage renal failure; —, not applicable. a Values in parentheses are 95% confidence intervals. b 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.
noma (2,23), the most common cause of death of HCVinfected 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 antibodypositive 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 con-
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founding 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.
PD and HD in HCV Patients: ESRF, Bose et al.
7. 8.
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. 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.
9. 10. 11.
12. 13. 14.
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.
15.
16. 17.
18.
19. References 1. Fabrizi F, Lunghi G, Ganeshan SV, Martin P, Messa P: Hepatitis C virus infection and the dialysis patient. Semin Dial 20: 416 – 422, 2007 2. Johnson DW, Dent H, Yao Q, Tranaeus A, Huang CC, Han DS, Jha V, Wang T, Kawaguchi Y, Qian J: Frequencies of hepatitis B and C infections among haemodialysis and peritoneal dialysis patients in Asia-Pacific countries: Analysis of registry data. Nephrol Dial Transplant 24: 1598 –1603, 2009 3. Sun J, Yu R, Zhu B, Wu J, Larsen S, Zhao W: Hepatitis C infection and related factors in hemodialysis patients in China: Systematic review and meta-analysis. Ren Fail 31: 610 – 620, 2009 4. Fabrizi F, Martin P: Health care-associated transmission of hepatitis B and C viruses in hemodialysis units. Clin Liver Dis 14: 49 – 60, 2010 5. Nakayama E, Akiba T, Marumo F, Sato C: Prognosis of antihepatitis C virus antibody-positive patients on regular hemodialysis therapy. J Am Soc Nephrol 11: 1896 –1902, 2000 6. Kalantar-Zadeh K, McAllister CJ, Miller LG: Clinical charac-
20.
21. 22. 23.
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teristics and mortality in hepatitis C-positive haemodialysis patients: A population based study. Nephrol Dial Transplant 20: 1662–1669, 2005 Stehman-Breen CO, Emerson S, Gretch D, Johnson RJ: Risk of death among chronic dialysis patients infected with hepatitis C virus. Am J Kidney Dis 32: 629 – 634, 1998 Wang SM, Liu JH, Chou CY, Huang CC, Shih CM, Chen W: Mortality in hepatitis C-positive patients treated with peritoneal dialysis. Perit Dial Int 28: 183–187, 2008 Sulowicz W, Radziszewski A, Chowaniec E: Hepatitis C virus infection in dialysis patients. Hemodial Int 11: 286 –295, 2007 Meyers CM, Seeff LB, Stehman-Breen CO, Hoofnagle JH: Hepatitis C and renal disease: An update. Am J Kidney Dis 42: 631– 657, 2003 Olmer M, Bouchouareb D, Zandotti C, de Micco P, de Lamballerie, X: Transmission of the hepatitis C virus in an hemodialysis unit: Evidence for nosocomial infection. Clin Nephrol 47: 263–270, 1997 Pereira BJ: Hepatitis C virus infection in dialysis: A continuing problem. Artif Organs 23: 51– 60, 1999 Zeuzem S, Teuber G, Lee JH, Ruster B, Roth WK: Risk factors for the transmission of hepatitis C. J Hepatol 24: 3–10, 1996 Chauveau P: Epidemiology of hepatitis C virus infection in chronic haemodialysis. Nephrol Dial Transplant 11[Suppl 4]: 39 – 41, 1996 Cendoroglo NM, Draibe SA, Silva AE, Ferraz ML, Granato C, Pereira CA, Sesso RC, Gaspar AM, Ajzen H: Incidence of and risk factors for hepatitis B virus and hepatitis C virus infection among haemodialysis and CAPD patients: Evidence for environmental transmission. Nephrol Dial Transplant 10: 240 – 246, 1995 Prati D: Transmission of hepatitis C virus by blood transfusions and other medical procedures: A global review. J Hepatol 45: 607– 616, 2006 Patel PR, Thompson ND, Kallen AJ, Arduino MJ: Epidemiology, surveillance, and prevention of hepatitis C virus infections in hemodialysis patients. Am J Kidney Dis 56: 371–378, 2010 Chou CY, Wang IK, Liu JH, Lin HH, Wang SM, Huang CC: Comparing survival between peritoneal dialysis and hemodialysis treatment in ESRD patients with chronic hepatitis C infection. Perit Dial Int 30: 86 –90, 2010 McDonald SP, Marshall MR, Johnson DW, Polkinghorne KR: Relationship between dialysis modality and mortality. J Am Soc Nephrol 20: 155–163, 2009 Fenton SS, Schaubel DE, Desmeules M, Morrison HI, Mao Y, Copleston P, Jeffery JR, Kjellstrand CM: Hemodialysis versus peritoneal dialysis: A comparison of adjusted mortality rates [see comments]. Am J Kidney Dis 30: 334 –342, 1997 Liem YS, Wong JB, Hunink MG, de Charro FT, Winkelmayer WC: Comparison of hemodialysis and peritoneal dialysis survival in The Netherlands. Kidney Int 71: 153–158, 2007 Heaf JG, Lokkegaard H, Madsen M: Initial survival advantage of peritoneal dialysis relative to haemodialysis. Nephrol Dial Transplant 17: 112–117, 2002 Fabrizi F, Martin P, Dixit V, Bunnapradist S, Dulai G: Metaanalysis: Effect of hepatitis C virus infection on mortality in dialysis. Aliment Pharmacol Ther 20: 1271–1277, 2004
Received: March 9, 2011 Accepted: August 7, 2011 Published online ahead of print. Publication date available at www.cjasn.org.
