Skip Navigation


NDT Advance Access originally published online on July 24, 2006
Nephrology Dialysis Transplantation 2006 21(10):2809-2813; doi:10.1093/ndt/gfl337
This Article
Right arrow Abstract Freely available
Right arrow FREE Full Text (PDF) Freely available
Right arrow All Versions of this Article:
21/10/2809    most recent
gfl337v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrow Search for citing articles in:
ISI Web of Science (23)
Right arrowRequest Permissions
Right arrow Disclaimer
Google Scholar
Right arrow Articles by Atta, M. G.
Right arrow Articles by Fine, D. M.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Atta, M. G.
Right arrow Articles by Fine, D. M.
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?

© The Author [2006]. Published by Oxford University Press on behalf of ERA-EDTA. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Antiretroviral therapy in the treatment of HIV-associated nephropathy

Mohamed G. Atta1,, Joel E. Gallant2, M. Hafizur Rahman1, Nagapradeep Nagajothi3, Lorraine C. Racusen4, Paul J. Scheel1 and Derek M. Fine1

1Department of Medicine, Division of Nephrology 2Division of Infectious Diseases, Johns Hopkins School of Medicine and the Johns Hopkins Hospital, Baltimore, Maryland 3Department of Medicine, Rosalind Franklin University of Medicine and Sciences, North Chicago, Illinois and 4Department of Pathology, Johns Hopkins School of Medicine and the Johns Hopkins Hospital, Baltimore, Maryland, USA

Correspondence and offprint requests to: Mohamed G. Atta, MD, MPH, Johns Hopkins University, Division of Nephrology, 1830 East Monument Street, Suite 416 Baltimore, Maryland-21205, USA. Email: matta1{at}jhmi.edu



   Abstract
Top
 Abstract
Introduction
 Methods
 Analysis
 Results
 Renal survival
 Discussion
 Acknowledgements
 References
 
Background. The effect of antiretroviral therapy (ART) on the clinical course of patients with human immunodeficiency virus (HIV)-associated nephropathy (HIVAN) is not well-established. This study was undertaken to further elucidate the potential benefit of ART in HIV-infected patients with documented HIVAN.

Methods. A cohort of 263 consecutive HIV-infected patients referred to the Johns Hopkins renal clinic from 1995 to 2004 was examined. Patients were included if they had biopsy-proven HIVAN and did not require dialysis within 1 month of their kidney biopsy. The cumulative probability of renal survival was calculated using the Kaplan–Meier method. Multivariate analysis was performed using the Cox regression method.

Results. Fifty-three patients among 152 biopsied patients had HIVAN. Among 36 patients who met the inclusion criteria, 26 were treated with ART (group I) and 10 patients were not (group II). Except for age, baseline demographics and clinical characteristics were similar in the two groups. Renal survival was significantly better in the group receiving ART by both univariate (P = 0.025) and multivariate analysis (overall adjusted hazard ratio = 0.30; 95% confidence interval 0.09–0.98; P < 0.05) for ART compared with no treatment.

Conclusions. Patients with biopsy-proven HIVAN treated with ART had better renal survival compared with patients who did not receive ART. HIVAN should be considered as an indication to initiate ART.

Keywords: ART; HAART; HIVAN; HIV; kidney biopsy; nephropathy



   Introduction
Top
 Abstract
 Introduction
Methods
 Analysis
 Results
 Renal survival
 Discussion
 Acknowledgements
 References
 
Human immunodeficiency virus (HIV)-associated nephropathy (HIVAN) is the leading cause of end-stage renal disease (ESRD) in patients with HIV infection [1]. It is characterized by glomerular capillary collapse, tubular microcystic dilatation and tubuloreticular inclusions, and if left untreated, it almost uniformly progresses to ESRD within weeks to months. Angiotensin-converting enzyme inhibitors (ACE-I) [2,3], corticosteroids [4] and antiretroviral agents [5,6] have been used in various combinations for the treatment of HIVAN.

There are several case reports describing the role of antiretroviral therapy (ART) in controlling or reversing the progression of renal failure in patients with HIVAN [7,8]. The widespread use of highly ART (HAART) has been shown to lead to a decrease in the incidence of HIVAN [9]. The progression of HIVAN to ESRD has also decreased since 1995, presumably reflecting the effect of HAART [10]. It has therefore been suggested that HIVAN should be considered an indication for HAART [11].

While these observational data suggest that ART is effective in the treatment of HIVAN, some studies have shown no benefit [12,13]. We performed a retrospective cohort study evaluating all patients with biopsy-proven HIVAN to determine the effect of ART on the clinical course of their renal disease.



   Methods
Top
 Abstract
 Introduction
 Methods
Analysis
 Results
 Renal survival
 Discussion
 Acknowledgements
 References
 
The medical records of 263 consecutive HIV-infected patients referred to the Johns Hopkins renal clinic from 1995 to 2004 were reviewed. The starting date in 1995 reflects the initiation of data collection. The Johns Hopkins Institutional Review Board approved the research protocol. HIVAN was defined based on the pathological findings of collapsing glomerulopathy, tubulointerstitial inflammation and podocyte injury. Over the period of the study, at least three renal pathologists were involved in examining the kidney biopsies. However, all pathology data were extracted by only one pathologist to apply the above criteria for the diagnosis of HIVAN. Treatment with ART was defined as initiation of at least one antiretroviral agent. Virological response to initiation of ART was defined as: (i) decrease in plasma HIV RNA by at least 1.5 log10 copies/ml or to <5000 copies/ml by 4 weeks [14,15] or (ii) decrease in HIV RNA to <500 copies/ml by 8–16 weeks [16] or (iii) decrease in HIV RNA to <50 copies/ml by 16–24 weeks [17]. Patients were classified as complete responders if they had the initial virological response as defined above, along with sustained suppression of viral load below 400 copies/ml for 24 weeks. Patients were considered as partial responders if viral load suppression was not sustained. Patients were excluded if they required dialysis within 1 month of renal biopsy. Patients were then divided into two groups: group I (patients treated with ART) and group II (patients not treated with ART).

Data on demographics (age, sex and race), comorbid conditions [diabetes, hypertension (defined as the use of antihypertensive medication at any time during the study period), hepatitis-B and hepatitis-C infection, injection drug use], HIVAN treatment (initiation of ACE-I, corticosteroids or antiretroviral agents within 3 months of biopsy and at anytime during the patient's follow up) and laboratory measurements at the time of renal biopsy (serum creatinine, urinary protein excretion by spot urinary protein to creatinine ratio or 24 h urine collection, CD4 count and plasma HIV RNA) were extracted from the patients’ medical record. Estimated glomerular filtration rate (GFR) was calculated based on the four variable modification of diet in renal disease (MDRD) equation [18]. In addition, serial viral loads and serum creatinine for each patient were collected for the duration of the follow up, where available.



   Analysis
Top
 Abstract
 Introduction
 Methods
 Analysis
Results
 Renal survival
 Discussion
 Acknowledgements
 References
 
Statistical analyses were performed using Stata Software version 8 (Stata Corporation, College Station, TX, USA). Both demographic and clinical characteristics of patients were compared between the group treated with ART and the group not treated. The mean values between the two groups were compared using Student's t-test for continuous variables and are presented as mean ± SD. Chi-square test was performed for comparison of discrete data.

Kaplan–Meier survival analysis was performed for calculating cumulative probability of renal survival for both ART-treated and untreated groups. Kaplan–Meier survival curves for each group were compared using a log-rank test statistic.

Relative risk of progression to ESRD, defined as requirement for dialysis support, between the ART-treated and untreated group was measured by hazard ratios (HRs) employing Cox proportional hazards models. Both unadjusted and adjusted HRs were obtained from bivariate and multivariate models to ascertain and compare the risk of ESRD. Only variables that are significant at 0.10 level in univariate analysis were included in the final multivariate model. Absolute P-values and 95% confidence intervals (CIs) for the difference between the groups were reported, where appropriate.



   Results
Top
 Abstract
 Introduction
 Methods
 Analysis
 Results
Renal survival
 Discussion
 Acknowledgements
 References
 
Characteristics of the patients
Among 263 HIV-infected patients with kidney disease, 152 underwent renal biopsy, of whom 53 (34.9%) had biopsy-proven HIVAN. None of these 53 patients had a diagnosis of classic focal segmental glomerulosclerosis. Of the 53 HIVAN patients, 16 (30%) required dialysis at the time of biopsy or within 1 month of biopsy and were excluded. As expected, excluded patients had more advanced kidney disease at the time of the biopsy, with higher serum creatinine and more significant proteinuria (Table 1). One patient was also excluded as follow-up time was not available. Among the 36 remaining patients, 26 (72.2%) were treated with ART, while the remaining 10 patients were not. In the ART-treated group, 17 patients were on HAART regimens, seven patients on combination ART and two patients on monotherapy.


View this table:
[in this window]
[in a new window]

  		Table 1. Baseline characteristics of the study patientsa

 
The treated group was significantly older but was otherwise demographically similar to the untreated group. The distribution of comorbidities, including hepatitis-B, hepatitis-C, hypertension and diabetes mellitus was not significantly different between groups. Mean serum creatinine was 4.65 mg/dl (±1.94) in the treated group and 7.75 mg/dl (±2.94) for the untreated group (P = 0.0008). However, there was no significant difference in the mean GFR between the two groups [20.3 ml/min/1.73 m2 (±12.9) and 13.6 ml/min/1.73 m2 (±13.5) in treated and untreated groups respectively, P = 0.18] (Table 1).



   Renal survival
Top
 Abstract
 Introduction
 Methods
 Analysis
 Results
 Renal survival
Discussion
 Acknowledgements
 References
 
The cumulative renal survival of patients included in the study was 14.2% at the end of the follow-up period (2962 days). Renal survival was significantly higher in the group treated with ART compared with the untreated group [18.1 vs 12.5%, P = 0.025 (log rank test)] (Figure 1A). Median renal survival was 552 days (18.4 months) for the treated group compared with 117 days (3.9 months) for the untreated group. The longest renal survival in the untreated group was 13 months, in a patient who was subsequently lost to follow-up, with the last documented serum creatinine being 6.6 mg/dl. Because this significant difference in the length of follow-up between the two groups may lead to survival bias (the probability of failure being higher with longer follow-up), analysis was performed considering the same follow-up time period for both groups, making the total duration of follow-up identical in all the censored and non-censored patients. The truncated analysis also demonstrated significantly better renal survival for the patients treated with ART (52.7 vs 12.5%, P < 0.05) (Figure 1B). None of the 36 patients studied died during the follow-up period.


Figure 1
View larger version (18K):
[in this window]
[in a new window]
[Download PowerPoint slide]
  		Fig. 1. (A) Kaplan–Meier estimate of renal survival in two groups of study patients (treated and not treated with ART). (B) Kaplan–Meier estimate of renal survival in study patients treated and not treated with ART (analysis time = 408 days).

 
A subgroup analysis was conducted to evaluate the effect of initiating ART early after renal biopsy and the relationship between virological suppression and renal survival. Data were examined based on whether ART was started within 3 months after the renal biopsy. Six patients were excluded from this analysis, as adequate information regarding their viral load or timing of initiation of ART was not available. Of the remaining 30 patients, there was a trend towards better renal survival among the 17 who started ART within 3 months of biopsy compared with those who did not (cumulative survival 37.5 vs 18.9%, P = 0.13). Figure 2 shows that among these 17 patients, there was a trend towards better renal survival in patients with complete virological response compared with those with a partial virological response (37.5 vs 8.8%, P = 0.12).


Figure 2
View larger version (17K):
[in this window]
[in a new window]
[Download PowerPoint slide]
  		Fig. 2. Kaplan–Meier estimates of renal survival in patients with complete and partial virological suppression.

 
Risk of ESRD (need for dialysis)
Both bivariate and multivariate analyses (adjusted for GFR, infection drug use, hepatitis-C and use of glucocorticoids) using Cox proportional hazards models demonstrated that progression to ESRD was significantly lower among ART-treated patients than those who were not treated (unadjusted HR = 0.36, P < 0.05; adjusted HR = 0.30, P < 0.05) (Table 2). Multivariate analysis also revealed that use of glucocorticoids was potentially protective, with a non-significant trend towards a lower risk of ESRD with glucocorticoid treatment (Table 2). Starting doses were mostly 1 mg/kg/day of prednisone, though data regarding total dose and duration of therapy was not available for analysis. The use of ACE-I was not associated with lower risk of ESRD, although the number of treated patients was small (only four patients), and the clinical impact could not be documented in this sample (P = NS). No patient was treated with an angiotensin receptor blocker.


View this table:
[in this window]
[in a new window]

  		Table 2. Unadjusted and adjusted HRs from Cox proportional hazards models

 


   Discussion
Top
 Abstract
 Introduction
 Methods
 Analysis
 Results
 Renal survival
 Discussion
Acknowledgements
 References
 
In our cohort study, the use of ART was associated with significantly better renal survival even after controlling for other treatment modalities such as the use of glucocorticoids. While a randomized control study would be the ideal way to assess the role of ART in the treatment of HIVAN, the efficacy of ART [19–25] and the poor prognosis of untreated HIV infection make it unethical to conduct such a trial.

In this study, treatment with ART was defined as initiation of at least one antiretroviral medication, which allowed inclusion of those treated in the pre-HAART era with one or two nucleoside analogue reverse transcriptase inhibitors as well as those treated with HAART. The trend towards improved renal survival in patients with complete as opposed to partial virological suppression (Figure 2, P = 0.12), suggests that the greatest benefit is associated with HAART in the setting of maximal virological suppression.

Although the survival benefit of ART in patients with HIV infection is well-established, its association with renal survival has been less clear. Several studies have suggested that ART could potentially slow the progression of HIVAN and other HIV-related renal diseases [7–9,26–29]. However, these studies were limited to case reports, and in several, the documentation of HIVAN was based on surrogate markers rather than biopsy. We have recently reported the limitations of using surrogate markers to establish the diagnosis of HIVAN [30,31] and believe that kidney biopsy is the gold standard for diagnosis. Furthermore, several studies found no renal benefit with ART. In the study by Szczech and colleagues [12], which included more than 2000 HIV-infected women, ART monotherapy, ART combination therapy and HAART were not associated with reduction in the risk of renal failure even when those with proteinuria were analysed separately. Again, biopsy-confirmed diagnoses were not used in this cohort. It is important to note, however, that kidney disease may have developed prior to the availability of HAART in many subjects in this cohort. In a study by Laradi and colleagues [13], a history of antiretroviral use was associated with poorer patient survival. However, this study included only patients from 1984 through 1996, before the introduction of HAART.

Human data and a murine transgenic model of HIVAN suggest that HIVAN is a direct result of viral gene expression [32–34]; therefore, it is plausible that ART could slow HIVAN progression by decreasing viral replication in the kidney. These data would suggest that biopsy-proven HIVAN is an indication for HAART, an approach that is not the current standard practice.

It is important to note the limitations of our study. First, we were unable to determine why some of the patients with biopsy-proven HIVAN were not treated with ART. Selection bias could have been introduced if such patients were more likely to be non-adherent or to be actively using drugs than those in the treated group. However, the similarities between the findings in this study and the recent cohort study by Szczech and colleagues [35] provide further support to our conclusion. Second, since this was a single-centre study at an academic institution with an active HIV clinic and because of the limited number of patients in the study, our patient population may differ significantly from those patients seen in other nephrology practices. Third, the inclusion of patients from the pre-HAART era, with a lower number on HAART, may limit the applicability of our results to today's regimens. However, the heterogeneity of antiretroviral regimens in this cohort would have been expected to bias the results towards the null.

In conclusion, this study provides further evidence that the HAART may slow the progression of HIVAN, which should be considered as an indication for HAART, independent of CD4 count, plasma HIV RNA, and HIV-associated symptoms and opportunistic conditions. This study emphasizes the importance of early diagnosis and treatment of HIVAN to prevent loss of renal function and ESRD.



   Acknowledgements
Top
 Abstract
 Introduction
 Methods
 Analysis
 Results
 Renal survival
 Discussion
 Acknowledgements
References
 
Preliminary data related to this manuscript was presented in an oral communication session during the American Society of Nephrology meeting in November 2005.

Conflict of interest statement. None declared.



   References
Top
 Abstract
 Introduction
 Methods
 Analysis
 Results
 Renal survival
 Discussion
 Acknowledgements
 References
 

  1. Winston JA, Burns GC, Klotman PE. (1998) The human immunodeficiency virus (HIV) epidemic and HIV-associated nephropathy. Semin Nephro 18:373–377.
  2. Burns GC, Paul SK, Toth IR, Sivak SL. (1997) Effect of angiotensin-converting enzyme inhibition in HIV-associated nephropathy. J Am Soc Nephrol 8:1140–1146.[Abstract]
  3. Klotman PE. (1998) Early treatment with ACE inhibition may benefit HIV-associated nephropathy patients. Am J Kidney Dis 31:719–722.[Medline]
  4. Eustace JA, Nuermberger E, Choi M, Scheel PJ Jr, Moore R, Briggs WA. (2000) Cohort study of the treatment of severe HIV-associated nephropathy with corticosteroids. Kidney Int 58:1253–1260.[CrossRef][ISI][Medline]
  5. Cook PP and Appel RG. (1990) Prolonged clinical improvement in HIV-associated nephropathy with zidovudine therapy. J Am Soc Nephrol 1:842.[ISI][Medline]
  6. Harrer T, Hunzelmann N, Stoll R, Baur A, Kalden JR. (1990) Therapy for HIV-1-related nephritis with zidovudine. Aids 4:815–817.[ISI][Medline]
  7. Scheurer D. (2004) Rapid reversal of renal failure after initiation of HAART: a case report. AIDS Read 14:443–447.[Medline]
  8. Kirchner JT. (2002) Resolution of renal failure after initiation of HAART: 3 cases and a discussion of the literature. AIDS Read 12:103–105 110–112.[Medline]
  9. Lucas GM, Eustace JA, Sozio S, Mentari EK, Appiah KA, Moore RD. (2004) Highly active antiretroviral therapy and the incidence of HIV-1-associated nephropathy: a 12-year cohort study. Aids 18:541–546.[CrossRef][ISI][Medline]
  10. Ross MJ and Klotman PE. (2002) Recent progress in HIV-associated nephropathy. J Am Soc Nephrol 13:2997–3004.[Free Full Text]
  11. Winston JA, Klotman ME, Klotman PE. (1999) HIV-associated nephropathy is a late, not early, manifestation of HIV-1 infection. Kidney Int 55:1036–1040.[CrossRef][ISI][Medline]
  12. Szczech LA, Gange SJ, van der Horst C, et al. (2002) Predictors of proteinuria and renal failure among women with HIV infection. Kidney Int 61:195–202.[CrossRef][ISI][Medline]
  13. Laradi A, Mallet A, Beaufils H, Allouache M, Martinez F. (1998) HIV-associated nephropathy: outcome and prognosis factors. Groupe d' Etudes Nephrologiques d’Ile de France. J Am Soc Nephrol 9:2327–2335.[Abstract]
  14. Ghani AC, Ferguson NM, Fraser C, et al. (2002) Viral replication under combination antiretroviral therapy: a comparison of four different regimens. J Acquir Immune Defic Syndr 30:167–176.[ISI][Medline]
  15. Maggiolo F, Migliorino M, Pirali A, Pravettoni G, Caprioli S, Suter F. (2000) Duration of viral suppression in patients on stable therapy for HIV-1 infection is predicted by plasma HIV RNA level after 1 month of treatment. J Acquir Immune Defic Syndr 25:36–43.[CrossRef][ISI][Medline]
  16. Demeter LM, Hughes MD, Coombs RW, et al. (2001) Predictors of virologic and clinical outcomes in HIV-1-infected patients receiving concurrent treatment with indinavir, zidovudine, and lamivudine. AIDS Clinical Trials Group Protocol 320. Ann Intern Med 135:954–964.[Abstract/Free Full Text]
  17. Yeni PG, Hammer SM, Hirsch MS, et al. (2004) Treatment for adult HIV infection: 2004 recommendations of the International AIDS Society-USA Panel. JAMA 292:251–265.[Abstract/Free Full Text]
  18. Levey AS GT, Kusek JW, Beck GJ, Group MS. (2000) A simplified equation to predict glomerular filtration rate from serum creatinine [Abstract]. J Am Soc Nephrol 11:155A.
  19. Gulick RM, Mellors JW, Havlir D, et al. (1997) Treatment with indinavir, zidovudine, and lamivudine in adults with human immunodeficiency virus infection and prior antiretroviral therapy. N Engl J Med 337:734–739.[Abstract/Free Full Text]
  20. Gulick RM, Mellors JW, Havlir D, et al. (2000) 3-year suppression of HIV viremia with indinavir, zidovudine, and lamivudine. Ann Intern Med 133:35–39.[Abstract/Free Full Text]
  21. Hammer SM, Squires KE, Hughes MD, et al. (1997) A controlled trial of two nucleoside analogues plus indinavir in persons with human immunodeficiency virus infection and CD4 cell counts of 200 per cubic millimeter or less. AIDS Clinical Trials Group 320 Study Team. N Engl J Med 337:725–733.[Abstract/Free Full Text]
  22. Ledergerber B, Egger M, Opravil M, et al. (1999) Clinical progression and virological failure on highly active antiretroviral therapy in HIV-1 patients: a prospective cohort study. Swiss HIV Cohort Study. Lancet 353:863–868.[CrossRef][ISI][Medline]
  23. Staszewski S, Morales-Ramirez J, Tashima KT, et al. (1999) Efavirenz plus zidovudine and lamivudine, efavirenz plus indinavir, and indinavir plus zidovudine and lamivudine in the treatment of HIV-1 infection in adults. Study 006 Team. N Engl J Med 341:1865–1873.[Abstract/Free Full Text]
  24. Hogg RS, Rhone SA, Yip B, et al. (1998) Antiviral effect of double and triple drug combinations amongst HIV-infected adults: lessons from the implementation of viral load-driven antiretroviral therapy. Aids 12:279–284.[CrossRef][ISI][Medline]
  25. Murphy RL, Gulick RM, DeGruttola V, et al. (1999) Treatment with amprenavir alone or amprenavir with zidovudine and lamivudine in adults with human immunodeficiency virus infection. AIDS Clinical Trials Group 347 Study Team. J Infect Dis 179:808–816.[CrossRef][ISI][Medline]
  26. Michel C, Dosquet P, Ronco P, Mougenot B, Viron B, Mignon F. (1992) Nephropathy associated with infection by human immunodeficiency virus: a report on 11 cases including 6 treated with zidovudine. Nephron 62:434–440.[ISI][Medline]
  27. Kimmel PL, Bosch JP, Vassalotti JA. (1998) Treatment of human immunodeficiency virus (HIV)-associated nephropathy. Semin Nephrol 18:446–458.[ISI][Medline]
  28. Wali RK, Drachenberg CI, Papadimitriou JC, Keay S, Ramos E. (1998) HIV-1-associated nephropathy and response to highly-active antiretroviral therapy. Lancet 352:783–784.[CrossRef][ISI][Medline]
  29. Ifudu O, Rao TK, Tan CC, Fleischman H, Chirgwin K, Friedman EA. (1995) Zidovudine is beneficial in human immunodeficiency virus associated nephropathy. Am J Nephrol 15:217–221.[ISI][Medline]
  30. Atta MG, Longenecker JC, Fine DM, et al. (2004) Sonography as a predictor of human immunodeficiency virus-associated nephropathy. J Ultrasound Med 23:603–610.[Abstract/Free Full Text]
  31. Atta MG, Choi MJ, Longenecker JC, et al. (2005) Nephrotic range proteinuria and CD4 count as noninvasive indicators of HIV-associated nephropathy. Am J Med 118:1288.e1221–1288.e1226.
  32. Barisoni L, Bruggeman LA, Mundel P, D’Agati VD, Klotman PE. (2000) HIV-1 induces renal epithelial dedifferentiation in a transgenic model of HIV-associated nephropathy. Kidney Int 58:173–181.[CrossRef][ISI][Medline]
  33. Conaldi PG, Biancone L, Bottelli A, et al. (1998) HIV-1 kills renal tubular epithelial cells in vitro by triggering an apoptotic pathway involving caspase activation and Fas upregulation. J Clin Invest 102:2041–2049.[ISI][Medline]
  34. Winston JA, Bruggeman LA, Ross MD, et al. (2001) Nephropathy and establishment of a renal reservoir of HIV type 1 during primary infection. N Engl J Med 344:1979–1984.[Free Full Text]
  35. Szczech LA, Gupta SK, Habash R, et al. (2004) The clinical epidemiology and course of the spectrum of renal diseases associated with HIV infection. Kidney Int 66:1145–1152.[CrossRef][ISI][Medline]
Received for publication: 18. 1.06
Accepted in revised form: 17. 5.06


Add to CiteULike CiteULike   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us    What's this?


This article has been cited by other articles:


Home page
 Am. J. Physiol. Renal Physiol.Home page
H. Ideura, K. Hiromura, N. Hiramatsu, T. Shigehara, S. Takeuchi, M. Tomioka, T. Sakairi, S. Yamashita, A. Maeshima, Y. Kaneko, et al.
Angiotensin II provokes podocyte injury in murine model of HIV-associated nephropathy
Am J Physiol Renal Physiol, October 1, 2007; 293(4): F1214 - F1221.
[Abstract] [Full Text] [PDF]

Home page
 CJASNHome page
C. M. Wyatt and P. E. Klotman
HIV-1 and HIV-Associated Nephropathy 25 Years Later
Clin. J. Am. Soc. Nephrol., July 1, 2007; 2(Supplement_1): S20 - S24.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow FREE Full Text (PDF) Freely available
Right arrow All Versions of this Article:
21/10/2809    most recent
gfl337v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrow Search for citing articles in:
ISI Web of Science (23)
Right arrowRequest Permissions
Right arrow Disclaimer
Google Scholar
Right arrow Articles by Atta, M. G.
Right arrow Articles by Fine, D. M.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Atta, M. G.
Right arrow Articles by Fine, D. M.
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?