The introduction of combined antiretroviral therapy (cART) has led to a considerable decline in deaths related to AIDS-defining illnesses. However, as patients live longer, there has been an increase in the number of deaths from other causes, such as end-stage liver and kidney disease, adverse effects of antiretroviral therapy, and other long-term complications (eg, diabetes or cardiovascular disease).1,2
The causes of HIV-associated chronic kidney disease are immune-mediated glomerulonephritis (GNF), HIV-associated nephropathy (HIVAN), drug-induced kidney disease, nonreversible acute renal failure, and thrombotic microangiopathy. White patients typically have GNF, whereas patients of African descent usually have HIVAN. Moreover, long-term survival and the increase in cardiovascular risk factors and cART-induced metabolic alterations could lead to increased prevalence of nephrosclerosis or diabetic nephropathy.3-6
As kidney disease progresses to end-stage renal disease (ESRD), renal replacement therapy—transplantation or dialysis—is recommended. Dialysis may serve as a bridge to transplantation or be the only alternative for patients excluded from renal transplantation. Renal transplantation is no longer a contraindication for HIV-infected patients, and experience in this field has grown in the last decade.7
Survival of HIV-infected patients on dialysis has increased in the last 2 decades. Early studies from the 1980s reported that survival of patients with newly diagnosed AIDS and ESRD was poor once hemodialysis had started, as most patients had advanced HIV infection that was often accompanied by opportunistic diseases.8,9 Survival of HIV-infected patients on dialysis began to improve considerably in the United States in the early 1990s. This improvement was consolidated in 1997 as a direct result of the widespread use of cART and better management and prophylaxis of opportunistic infections but also thanks to technical advances in dialysis delivery.10 A few studies that have evaluated survival rates and predictors of survival among HIV-infected patients on dialysis in the cART era are almost all retrospective and based on national registries or databases. In addition, they were performed in the United States, where the characteristics of the HIV-infected population on dialysis are different from those of European patients on dialysis.11-13
The aim of the present study was to determine the survival rates of HIV-infected patients who started dialysis in the cART era, to compare them with a matched HIV-negative cohort, and to determine HIV-associated risk factors for mortality.
MATERIALS AND METHODS
Design and Setting
A national, multicenter, and retrospective cohort study with matching in cooperation with the following Spanish societies: the Spanish Society of Nephrology (Sociedad Española de Nefrología), the AIDS Study Group [Grupo de Estudio de Sida (GESIDA)] of the Spanish Society of Infectious Diseases and Clinical Microbiology (Sociedad Española de Enfermedades Infecciosas y Microbiología Clínica), the GESIDA Clinical Trials Agency (Agencia de Ensayos Clínicos-GESIDA), and the Infectious Diseases in Solid Organ Transplant Recipients Study Group (GESITRA) of the Sociedad Española de Enfermedades Infecciosas y Microbiología Clínica.
The authors previously described the clinical and epidemiologic features of a Spanish cohort of HIV-infected patients on dialysis in 2006, including 35 dialysis units and 81 HIV-infected patients on dialysis.14 A questionnaire was sent to these dialysis centers requesting information on all HIV-infected patients who started dialysis between January 1999 and December 2006, regardless of their condition at the time of the survey (alive and still under dialysis, dead, transplant recipient, or lost to follow-up). To perform a competing risk analysis, additional follow-up information—patient health status and graft condition at the time of the survey—was requested for all transplant recipients.
Each HIV-infected patient was matched with 1 HIV-negative patient following 5 criteria: same dialysis center, age (±5 years), year of starting dialysis (±3 years), race, and sex. When it was not possible to find HIV-negative patients meeting all 5 criteria, we accepted fulfillment of at least the first 3 criteria and excluded race and sex.
We recorded demographic data and data related with chronic kidney disease, HIV infection, hepatitis coinfection, renal transplantation, and previous comorbidity (bacterial infectious complications and cardiovascular events).
The etiology of ESRD was classified according to the criteria of the European Renal Association-European Dialysis and Transplant Association,15 and patients with a clinical or histological diagnosis of cirrhosis were classified using the Child-Pugh classification.
Quantitative variables are expressed as median and interquartile range. Qualitative variables are expressed as the number of patients and percentages. The χ2 or Fisher exact tests were used to compare qualitative variables. The t test was used to compare quantitative variables. Statistical significance was set at 0.05.
A Kaplan-Meier survival analysis was performed. Patients who were withdrawn from dialysis (due to death or renal transplantation) were censored. Mortality risk factors were tested using univariate analysis (log-rank test for qualitative variables, Cox model for quantitative variables). The results were expressed as hazard ratios (HRs) [HR; 95% confidence interval (CI)]. All significant values with P <0.1 in the univariate analysis and with <20% of missing data were tested in a multivariate Cox regression model based on both stepwise and backward selection. The significance level for entering effects and the significance level for removing effects were set at 0.05. The data included in the univariate analysis were age (at the onset of dialysis and at HIV diagnosis), sex, ethnicity (black vs white), prior injection drug use, prior AIDS events, CD4+ T-cell count (at the onset of dialysis and last count), HIV RNA viral load, cART, modality and duration of dialysis, hepatitis coinfection, diabetes mellitus, cardiovascular events, and prior infectious complications. Finally, a competing risk model was also constructed.16 Statistical calculations were performed using SPSS Release 11.0.1. 2001. (SPSS Inc, Chicago, IL) and R (R Foundation for Statistical Computing, Vienna, Austria).17
Twenty-one of 35 centers participated in the study, and 19 of them had HIV-infected patients with the inclusion criteria (18 hospital dialysis units and 1 outpatient clinic). We identified 66 HIV-infected and 66 HIV-negative patients on dialysis. Their baseline characteristics are shown in Table 1.
Sociodemographic Parameters and Comorbidities
Most patients were white men (only 4 HIV-infected patients were black) of young age. In the HIV-infected group, median age at the time of HIV diagnosis was 33 (28-40) years.
The number of patients with diabetes was similar in both groups, but prior cardiovascular events were significantly more frequent in HIV-negative patients. The number of prior bacterial infections was higher in the HIV-infected group. The frequency of peritonitis was similar, but catheter-related infections were significantly more frequent in HIV-infected patients. Microbiologic isolates were not collected in the present study.
ESRD, Dialysis, and Renal Transplantation
The most frequent modality was hemodialysis. Eight patients from the HIV-infected group and 11 from the HIV-negative group switched modality during follow-up. All centers except 1 used both dialysis modalities and the remaining centers used only hemodialysis. All centers reported that patients received information regarding the benefits and risks of the dialysis modality, and with the exception of a major contraindication in 1 case, the final decision was taken by the patient. The most frequent cause of ESRD in HIV-infected patients was GNF. HIV-associated conditions such as HIVAN and thrombotic microangiopathy were only reported in 4 (6.1%) cases and 3 (4.5%) cases, respectively. All patients with HIVAN were black. The proportion of HIV-infected patients who had received a renal transplant or were included on the waiting list was significantly lower than in the HIV-negative group. Fifty-five (83%) HIV-infected patients were excluded from transplantation for different reasons, the most frequent being HIV infection (25 cases, including low CD4+ T-cell count, high HIV-1 RNA viral load, or prior excluding AIDS events) followed by liver disease (9 cases).
The median time from HIV diagnosis was 11.6 (6.8-15.8) years, and the most common route of HIV transmission was former intravenous drug use in 38 (57.6%) patients, followed by sexual transmission in 18 (27%). Thirty-five (53%) patients had 67 prior AIDS events, the most frequent being infection by Mycobacterium tuberculosis (n = 17), herpes zoster (n = 8), and esophageal candidiasis (n = 7). Forty-nine (74.2%) patients were receiving cART at the start of dialysis and 60 (90.9%) at the time of the survey. In both cases, the most frequent regimens were protease inhibitor (PI)-based and nonnucleoside reverse transcriptase inhibitor-based combinations. At the start of dialysis, the median CD4+ T-cell count was 220 (139-413) cells per cubic millimeter and 47% had more than 200 cells per cubic millimeter. At the time of the survey, the median T-cell count was 355 (189-525) cells per cubic millimeter, 63.6% patients were above 200 cells per cubic millimeter, and 42 (63.6%) had an undetectable HIV RNA plasma viral load.
Viral Hepatitis Coinfection
Fifty (75.8%) HIV-infected patients and 7 (10.6%) HIV-negative patients were coinfected with hepatitis C virus (HCV) (P < 0.001). Median time from diagnosis of hepatitis was 8.5 (2.0-16.3) years and 4.7 (4.1-11.8) years in the HIV-infected and HIV-negative groups, respectively. HCV RNA viral load was reported for 29 HIV-infected patients and was detectable in 20 (69%). Information on genotype was reported for 20 patients, the most frequent genotype being 1 (n = 10; 50%). Thirty-four (68%) HIV-infected patients were asymptomatic, and the remaining 16 were described as cirrhotic (most frequent Child-Pugh score was A). Only 2 patients had received specific antiviral therapy. Four (6.1%) patients had hepatitis B virus coinfection (hepatitis B surface antigen positive) in both HIV-infected and HIV-negative groups. All patients were described as asymptomatic, and 2 HIV-infected patients were receiving specific antiviral treatment. In the HIV-infected group, 5 of 50 (10%) HCV-coinfected patients were on the transplant waiting list, a significantly lower proportion than in the HIV-monoinfected group [6 of 16 (37.5%)] (P = 0.018).
Outcome and Causes of Death
After a median follow-up of 3.1 years, 25 (38%) HIV-negative and 3 (4.5%) HIV-infected patients underwent a renal transplant. Thirty-eight (58%) HIV-negative patients and 37 (56%) HIV-infected patients were alive on dialysis. Twenty-one (32%) HIV-infected patients and only 1 (1.5%) HIV-negative patient died. The causes of death are shown in Table 1. In the HIV-infected group, the most frequent was bacterial infection, but no cases of bacterial peritonitis or opportunistic infections were reported.
Survival Estimates and Competing Risk Analysis
Survival (95% CI) rates at 1, 3, and 5 years for HIV-infected patients were 95.2% (89.9%-100%), 71.7% (59.7%-83.7%), and 62.7% (46.6%-78.8%), respectively. Survival for HIV-negative patients at 5 years was 94.4% (83.8%-100%) (P < 0.001). Figure 1A shows that the Kaplan-Meier survival estimate was significantly better in the HIV-negative dialysis patients than in HIV-infected ESRD patients. HIV infection was associated with an increased risk of death [HR, 19.4 (95% CI: 2.6-144.3)] (P = 0.0038).
Competing risk results are shown in Figures 2A and 2B. The cumulative incidence function for death was significantly higher in the HIV-infected group (P < 0.001). In contrast, the cumulative incidence function for transplant was higher in the HIV-negative group (P < 0.001). HIV infection was associated with an increased competing risk of death (HR, 26.4) (P = 0.0015).
Univariate and Multivariate Analysis
Not being on effective cART and being on peritoneal dialysis (vs hemodialysis) were the main mortality risk factors in the univariate analysis (Table 2). We did not find significant differences in baseline characteristics among HIV-infected patients stratified by dialysis modality (Table 3). However, patients on peritoneal dialysis showed a nonsignificant trend toward more prior cardiovascular events and diabetes mellitus than hemodialysis patients. Survival was significantly better among patients on hemodialysis than among patients on peritoneal dialysis (P = 0.016, log-rank) (Fig. 1B). Multivariate analysis showed being on effective cART (odds ratio 0.39, 95% CI: 0.16-0.97; P = 0.043) and being on peritoneal dialysis (vs hemodialysis) (odds ratio 2.88, 95% CI: 1.16-7.17; P = 0.023) to be independently associated with mortality. We also analyzed the 21 HIV-infected patients on peritoneal dialysis and compared their characteristics according to health status (see Table, Supplemental Digital Content 1, http://links.lww.com/QAI/A190). We only found significant differences with the antiretroviral regimen. Almost all patients on a PI-based regimen were dead, and all patients on a nonnucleoside reverse transcriptase inhibitor-based regimen were alive (P = 0.03).
Few studies have analyzed the outcome of HIV-infected patients on dialysis. With the exception of an isolated study performed in France,18 all the studies have been performed in the United States and have compared the outcome of HIV-infected patients on dialysis with national registries or databases from the general dialysis population. In the present study, we compared the outcome of HIV-infected patients on dialysis with a matched cohort of HIV-negative patients. All previous studies except 1 are retrospective cohort studies, and the French study is the only prospective study. Ours is the second survival study of HIV-infected patients on dialysis performed in Europe in the cART era and the first including patients on hemodialysis and peritoneal dialysis.
Survival rates of HIV-infected patients on dialysis have improved in recent years. Even after performing a competing risk analysis, we found that HIV infection was associated with an increased risk of death. The survival rate of HIV-infected patients on dialysis was lower (62.7%) than that of matched HIV-negative patients (94.4%) and lower than the 5-year survival rate reported by Mazuecos et al19 (95%) in a series of 20 renal transplants performed in Spain between 2001 and 2009. Data from the US Renal Data System showed that 12- and 24-month survival rates among HIV-negative patients were 87% and 79%, respectively, compared with 58% and 41% among HIV-infected patients.10 The 5-year survival rate found in our study is similar to that reported in a recent epidemiological study performed in the United Kingdom between 1998 and 2007 (70.3% survival at 5 years).20 In contrast, Rodriguez et al11 found a very low 5-year survival rate (9%), probably because patients from the pre-cART era were also included in the analysis. Studies including patients from the pre-cART era usually showed poor survival rates (30%-41%) at 2 years of follow-up.9-11 The French study found better survival rates at 1 and 2 years (93.8% and 89.4%, respectively), which are similar to our findings.18 However, not all studies from the cART era have reported an improvement in survival rates. Atta et al13 revealed very poor survival rates among HIV-infected African American patients who initiated dialysis in the cART era (63% and 43% at 1 and 2 years, respectively). This cohort had high rates of poverty and substance abuse and a low frequency of cART use, characteristics which were similar to those observed during the pre-cART era.
A few data are available on causes of death among HIV-infected patients on dialysis, although bacterial infections are the most frequently reported.11,18 In the present study, bacterial infections were the leading cause of death, followed by myocardial infarction and sudden death. Infections were also the most frequent cause of death (54%) in the US study by Rodriguez et al,11 followed by drug overdose or noncompliance with dialysis (16%), cachexia (9%), and cardiovascular events (<5%). The main causes of death reported by Tourret et al18 were bacterial infections (31.8%), sudden death (18.2%), and cancer (13.6%). In our study, 2 patients died as a consequence of peritoneal sclerosis, which is a rare but serious complication of peritoneal dialysis.21 To our knowledge, only 2 cases have been reported in HIV-infected patients.22,23 Existing knowledge does not allow us to directly relate HIV infection with the etiology of this rare complication, but further studies should confirm whether HIV-infected patients are at greater risk of developing peritoneal sclerosis.
A few studies have evaluated the predictors of survival of HIV-infected patients with ESRD. Low CD4+ T-cell counts, high HIV RNA levels, and prior AIDS events have been associated with an increased risk of death.11,13,18 cART is successful in suppressing viral load in HIV-infected patients on dialysis, and our and previous studies have shown that survival of HIV-infected dialysis patients on cART is better than that of patients not receiving or receiving suboptimal antiretroviral therapy.12,13,18 For this reason, achieving a suppressed viral load under cART regimens must be a mandatory objective in these patients.
Data regarding the role of peritoneal dialysis in the treatment of HIV-infected patients with ESRD are limited. Small studies from the pre-cART era did not find dialysis modality to be a factor for survival.24 Using the US Renal Data System database (1995-1999), Ahuja et al25 did not find differences in survival between HIV-infected patients on hemodialysis and those on peritoneal dialysis. However, the major limitations of this study were the lack of information on comorbidities, plasma viral load, and CD4+ T-cell count.25 We found that patients on peritoneal dialysis had a higher risk of mortality than patients on hemodialysis. A recent retrospective matched-pair cohort study, including non-HIV-infected patients who initiated dialysis in the United States in 2003, found that mortality in patients with cardiovascular disease and diabetes was higher among those undergoing peritoneal dialysis.26 Our comparison of baseline characteristics revealed that the peritoneal dialysis group had a nonsignificant higher proportion of patients with diabetes mellitus and prior cardiovascular events, which could probably explain—in part—this excess mortality. On the other hand, we found a slightly lower proportion of patients with effective cART in the peritoneal dialysis group. Furthermore, it is noteworthy that almost all patients on peritoneal dialysis who died were receiving a PI-based regimen. It is unknown whether antiretroviral dosing and efficacy of cART in patients on peritoneal dialysis is comparable with the dosing and efficacy of cART in patients on hemodialysis. Recent studies in the general population undergoing peritoneal dialysis have demonstrated a strong predictive association between daily peritoneal ultrafiltration and patient survival27 and between the rate of decline of residual renal function and all-cause mortality.28 These factors were not evaluated in the present study.
Another major concern in peritoneal dialysis is the increased incidence of peritonitis among HIV-infected patients, although published data on this issue are controversial. The studies that found a higher risk of peritonitis and more cases of peritonitis attributed to Pseudomonas species or fungi were performed before cART became available. In some cases, this risk could have been due to low socioeconomic status and/or injection drug use.24,29
Until further studies are conducted, the criteria for selecting the dialysis modality should be similar to those applied to other patients with ESRD, although peritoneal dialysis should be indicated with caution in HIV-infected patients with prior cardiovascular events and/or diabetes mellitus.
White patients typically have non-HIVAN GNF, whereas black patients in the same centers usually have HIVAN.30 We found the most frequent etiology of chronic kidney disease to be non-HIVAN GNF, which is consistent with the racial distribution of our study. Stratification by race revealed that black patients accounted for 65% of the sample in a French study18 and a British study20; this percentage is notably higher than that of our study.
A few data have been published on the frequency or clinical features of catheter-related bacteremia in HIV-infected dialysis patients, and previous studies have reported similar frequencies of catheter-related infection in HIV-infected and HIV-negative patients.31,32 In our study, catheters were used for vascular access in 44% of HIV-infected patients and 13.5% of HIV-negative patients (probably because of vascular access difficulties in former drug users) and this is the reason why more catheter-related infections were found in the HIV-infected group.
Information regarding HIV-infected patients on the renal transplantation waiting list is scarce. In our study, HIV-infected patients were less frequently included on the transplant waiting list than HIV-negative patients. Eleven (16.7%) were included on the waiting list and the remaining 55 (83.3%) were excluded for different reasons, the most frequent being poor control of HIV infection. We also observed that HCV coinfection was a major limitation for inclusion on the waiting list (only 5 of the 50 coinfected patients were included). One of the largest studies performed on this issue retrospectively reviewed 309 potentially eligible HIV-infected patients at a single US institution and found that only 20% of HIV patients were listed or had received a transplant compared with 73% of HIV-negative patients evaluated over the same period. The most common reasons for failure to proceed for full evaluation were CD4+ T-cell count and viral load data not provided at the initial evaluation (35%) and CD4+ T-cell count and viral load not meeting eligibility criteria (21%).33 In Europe, recent data from the EuroSIDA cohort study showed that a poor control of HIV infection, cardiovascular diseases, and diabetes were the most frequent reasons for exclusion.34 A recent 3-year follow-up results of a prospective and multicenter US trial including 150 patients showed that renal transplantation is highly feasible in HIV-infected recipients.35 For this reason, all ESRD HIV-infected patients should be carefully evaluated for transplantation36 and dialysis must be only considered an alternative therapy for those excluded from transplantation.
In conclusion, survival of HIV-infected patients on dialysis has improved in the past few years, although it remains lower than that of HIV-negative patients. Poor control of HIV is a risk factor for increasing mortality and a limitation for transplantation. Maintaining a suppressed viral load under cART is the key to improving survival. Large-scale studies must confirm whether peritoneal dialysis is a risk factor for mortality in HIV-infected patients.
We thank the Conference of Retroviruses and Opportunistic Infection Organization for the Young Investigator Award given to Dr. J. C. Trullas. We also thank the GESIDA, the Sociedad Española de Enfermedades Infecciosas y Microbiología Clínica, the Sociedad Española de Enfermedades Infecciosas y Microbiología Clínica-GESIDA Foundation (Beatriz Moyano, Herminia Esteban, Esther Aznar, Elena Barquilla), the Sociedad Española de Nefrología, the Sociedad Española de Trasplante, and all participating centers and our patients.
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List of investigators of the Spanish HIV Infection in Dialysis Study Group: A. Martínez-Castelao and Xavier Fulladosa, Hospital Universitari de Bellvitge, Hospitalet del Llobregat, Barcelona, Spain; R. Jofre, Hospital Universitario Gregorio Marañón, Madrid, Spain; M. Rivera, Hospital Ramón y Cajal, Madrid, Spain; S. Ros, Hospital Carlos Haya, Málaga, Spain; J. M. Miró, F. Cofan, A. Moreno, Carlos Cervera, Iñaki Perez, Francesc Maduell, and Jose Maria Gatell, Hospital Clínic-IDIBAPS, Universitat de Barcelona, Barcelona, Spain; J-.C. Trullàs, Hospital Sant Jaume, Olot, Girona, Spain; Ma Fuensanta Moreno, Hospital Príncipe de Asturias de Alcalá de Henares, Madrid, Spain; Olga González-Peña, Hospital de Basurto, Bilbao, Vizcaya, Spain; Ma Luisa Muñiz Gómez, Hospital de Cruces, Baracaldo, Vizcaya, Spain; José Antonio Herrero Calvo, Hospital Clínico San Carlos, Madrid, Spain; J. Martínez-Ara and Juan González-García, Hospital Universitario La Paz, Madrid, Spain; Rafael Alvarez Lipe, Hospital Lozano Blesa, Zaragoza, Spain; Jesús Modol and Alicia Pérez, Centro Althaia Hospital de Manresa, Manresa, Barcelona, Spain; Jesús Ma Núñez, Hospital Clínico Universitario de Valladolid, Valladolid, Spain; G. Barril and Martin Giorgi, Hospital Universitario La Princesa, Madrid, Spain; Rafael García Ramón, Hospital Clínico Universitario de Valencia, Valencia, Spain; Felipe Sarró, Hospital Arnau de Vilanova, Lleida, Spain; María Dolores Albero, Hospital de Alcoy, Alicante, Spain; Joaquín de Juan Ribera, Centro de Diálisis ASHDO, Elche, Alicante, Spain; and José María Lamas Barreiro, Hospital de Meixoeiro, Vigo, Spain. Steering Committee: J. M. Miró (Chair), J. C. Trullás, F. Cofan, A. Moreno, C. Cervera, I. Pérez, B. Mahillo, G. Barril, F. J. Burgos, J. González-García.
Coordinating Center Staff: B. Moyano, H. Esteban, E. Barquilla, J. González-García, and E. Aznar from the Sociedad Española de Enfermedades Infecciosas y Microbiología Clínica-GESIDA Foundation. Methodological Committee: J. M. Miró, J. C. Trullás, I. Perez, C. Cervera, A. Moreno, and F. Cofán.
HIV infection; end-stage renal disease; dialysis; survival
Supplemental Digital Content
© 2011 Lippincott Williams & Wilkins, Inc.