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AIDS:
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Highly active antiretroviral therapy and the incidence of HIV-1-associated nephropathy: a 12-year cohort study

Lucas, Gregory Ma; Eustace, Joseph Aa; Sozio, Stephena; Mentari, Evelyn Ka; Appiah, Kofi Ab; Moore, Richard Da

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From the aJohns Hopkins University, Baltimore and the bGood Samaritan Hospital, Baltimore, Maryland, USA.

Correspondence to Gregory M. Lucas, MD, 1830 E. Monument Street, Room 421, Baltimore, MD 21287, USA

Tel: +1 410 614 0560; fax: +1 410 955 7889; e-mail: glucas@jhmi.edu

Received: 19 June 2003; revised: 28 August 2003; accepted: 17 September 2003.

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Abstract

Objective: to assess temporal changes in the incidence of human immunodeficiency virus-1-associated nephropathy (HIVAN), and the association with use of highly active antiretroviral therapy (HAART).

Methods: HIVAN incidence and risk factors were assessed in 3976 HIV-1-infected individuals followed in clinical cohort in Baltimore, Maryland, USA from 1989 to 2001. The incidence of HIVAN, defined by biopsy or a conservative uniformly applied clinical coding protocol, was expressed in terms of person-years, and Poisson regression was used for multivariate analysis.

Results: Ninety-four patients developed HIVAN over the course of the study for an incidence of 8.0 per 1000 person-years [95% confidence interval (CI), 6.5 to 9.8]. African American race and advanced immunosuppression were strongly associated with HIVAN risk. HIVAN incidence declined significantly in 1998–2001 compared with 1995–1997. Among patients with a prior diagnosis of AIDS, HIVAN incidence was 26.4, 14.4, and 6.8 per 1000 person-years in patients not receiving antiretroviral therapy, treated with nucleoside analogue therapy only, or treated with HAART, respectively (P < 0.001 for trend). In multivariate analysis, HIVAN risk was reduced 60% (95% CI, −30 to −80%) by use of HAART, and no patient developed HIVAN when HAART had been initiated prior to the development of AIDS.

Conclusion: HAART was associated with a substantial reduction in HIVAN incidence. Additional follow-up will be needed to determine if renal damage in susceptible individuals is halted or merely slowed by HAART, particularly when control of viremia is incomplete or intermittent.

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Introduction

Human immunodeficiency virus-1-associated nephropathy (HIVAN) is characterized by high-grade proteinuria and rapid progression to end-stage renal disease (ESRD) [1]. ESRD incurs high cost [2], and has been associated with very high mortality in HIV-1-infected individuals in the past [3,4], although recent reports suggest improved survival in the era of highly active antiretroviral therapy (HAART) [5]. HIVAN occurs overwhelmingly in individuals of African or Haitian descent [6] with advanced HIV-1 disease [7], and is the third leading cause of ESRD in African Americans between the ages of 20 and 64 years [8]. As African Americans constitute only 13% of the US population, but accounted for an estimated 54% of new HIV infections in 2000 [9], some experts have described HIVAN as a looming urban epidemic [10].

Case reports and case series have suggested that HAART [11–14], corticosteroids [15,16], and angiotensin-converting enzyme inhibitors [17] may stabilize renal function and delay progression to ESRD in patients with HIVAN. However, we are aware of no longitudinal cohort studies evaluating changes in HIVAN incidence over the period of widespread dissemination of HAART. Such data have important implications for resource planning, research on screening strategies for detecting early stage HIVAN, and new treatments. We evaluated factors associated with development of HIVAN from 1989–2001 in a large, predominantly African American cohort of HIV-1-infected individuals in Baltimore, Maryland, USA.

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Methods

Database and case definition

The Johns Hopkins HIV Clinic provides longitudinal care to a large number of HIV-1-infected individuals in the Baltimore area. All patients enrolling in the clinic undergo a detailed baseline assessment, with collection of demographic, social, behavioral, and clinical information. A comprehensive panel of blood tests and a urinalysis is obtained at clinic enrollment. Serum chemistries, renal function tests, hepatic function tests, complete blood count, CD4 cell counts, and HIV-1 RNA (after 1995) are routinely monitored at 3-month intervals (or more frequently if clinically indicated) following enrollment.

An observational clinical database comprising over 4000 patients who have been treated in the clinic was established in 1989 [18]. Information from clinical records is reviewed and abstracted by professionally trained technicians onto structured data collection forms, then entered into an automated database. The clinic medical records, the main hospital medical record and various institutional automated databases (e.g., laboratory, radiology, pathology, discharge summaries) are abstracted. Comprehensive demographic, clinical, laboratory, pharmaceutical, and psychosocial data are collected at times corresponding to enrollment in the clinic and at 6-month intervals thereafter. The Johns Hopkins Institutional Review Board approved this clinical cohort study.

According to a protocol, consistently applied since cohort inception, data abstractors identified patients as having possible HIVAN if this diagnosis was considered at any time in the clinical or pathological records, or if patients had progressive renal disease of unknown etiology. Patients who underwent a renal biopsy were also identified from an automated institutional pathology database.

We subsequently conducted a detailed medical record review of all patients initially identified as having possible HIVAN. Information was recorded on structured data collection forms and included, relevant laboratory tests, renal imaging studies, use of nephrotoxic drugs, other diagnoses relevant to renal disease, and nephrology consultant findings. HIVAN cases were categorized as biopsy defined if characteristic histopathologic findings were documented [19]. Because many patients with progressive renal disease never underwent renal biopsy, HIVAN cases were categorized as clinically defined if no biopsy had been performed and the patient had (1) proteinuria in excess of 3 g/24 h or a urine protein/creatinine concentration ratio above 2.5, and (2) a subacute progressive increase in serum creatinine. Clinically defined HIVAN cases were excluded by the presence of: (1) acute renal failure, with return to a stable baseline serum creatinine below 1.5 mg/dl; (2) history of collagen vascular disease, diabetes of more than 5 years duration, uncontrolled hypertension, or other underlying disease likely to cause chronic renal failure; or (3) detectable cryoglobulinemia, serum complement levels below the lower limit of normal, bilateral small kidneys on sonogram, or a urine sediment containing red blood cell casts.

Only incident HIVAN cases were included in the analysis. Patients who entered the cohort with a confirmed or possible diagnosis of HIVAN or advanced renal disease were excluded. The date of HIVAN onset was defined as the date that renal disease was first documented as a problem in patients’ clinical records.

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Statistical analysis

Demographic, clinical, and laboratory data were compared in the general clinic population, patients with biopsy defined HIVAN, and patients with clinically defined HIVAN. Categorical variables were compared with Fisher's exact test and continuous variables with the Wilcoxon rank-sum test. HIVAN incidence rates were expressed as cases per 1000 person-years. Sex, race, and HIV-1 exposure group were included as fixed covariates. Age, calendar time, AIDS status, and use of antiretroviral therapy were included as time-dependent covariates. AIDS was defined according to the 1993 Centers for Disease Control and Prevention guidelines [20], which included CD4 cell count < 200 × 106 cells/l. Antiretroviral therapy was categorized hierarchically as none, nucleoside reverse transcriptase inhibitor (NRTI) only, or HAART. HAART was defined as use of a protease inhibitor, a non-nucleoside reverse transcriptase inhibitor, or abacavir, in a regimen including three or more antiretroviral agents. Once a given level of therapy had been used for more than 30 days, patients were categorized at that level. Factors associated with HIVAN incidence were evaluated in univariate and multivariate Poisson regression models. Potential interactions between variables were assessed by stratification and combining terms in multivariate models.

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Results

Over 11 732 person-years of follow-up from 1989 to 2001, 315 potential HIVAN cases were identified during cohort data abstraction, of which 313 (99%) had records available for review. Of those, eight (3%) had been miscoded, 29 (9%) had an acute renal condition that resolved completely, 31 (10%) were lost to follow-up or died before renal disease could be further characterized, 75 (24%) had biopsy or clinical evidence most consistent with a renal diagnosis other than HIVAN, 35 (11%) had renal disease of unknown etiology, but criteria for HIVAN were not met, 105 (34%) met criteria for clinically defined HIVAN, and 30 (10%) had biopsy-defined HIVAN. Of the 135 patients with HIVAN, 94 (23 biopsy defined and 71 clinically defined) developed renal disease following enrollment in the clinical cohort (incident cases) and were included in the analysis. Calendar period was not significantly associated with the proportions of reviewed cases that were ultimately categorized as biopsy defined HIVAN, clinically defined HIVAN, or excluded (data not shown). Of the 71 patients in the cohort who underwent a renal biopsy, the frequencies of histopathological findings were as follows: 30 (42%) showed HIVAN, 18 (25%) had an alternative form of glomerulonephritis other than HIVAN, eight (11%) were non-diagnostic, six (8%) had diabetic glomerulosclerosis, two biopsies showed hypertensive nephrosclerosis, two interstitial nephritis, two acute tubular necrosis, and one showed amyloid, one lymphoma and one obstructive uropathy.

In comparison with the general clinic population, baseline factors associated with development of HIVAN included, African American race, lower CD4 cell count, higher HIV-1 RNA level (in the subset followed after 1995, when this assay became available), history of injection drug use, and not being a man who has sex with men (Table 1). Hepatitis C antibody positive status (in the subset of 2960 patients in whom results from this assay were available) was associated with HIVAN in univariate analysis (Table 1), but did not remain significantly associated with HIVAN after adjustment for race [rate ratio (RR) for hepatitis C antibody positive versus negative, 1.5; 95% confidence interval (CI), 0.9–2.4]. There were no statistically significant differences in covariates between patients with biopsy defined and clinically defined HIVAN (Table 1).

Table 1
Table 1
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The HIVAN incidence rates were 10.1 and 1.1 per 1000 person-years in African American and white patients, respectively (RR, 9.0; 95% CI, 2.8–28.4). Patients with AIDS developed HIVAN at a rate of 12.5 compared to 3.1 per 1000 person-years in patients without AIDS (RR, 4.1; 95% CI, 2.4–6.9). Compared with prior calendar periods, the incidence of HIVAN declined in 1998 through 2001, in both AIDS-defined and non-AIDS defined individuals (Fig. 1). In a Poisson regression model, controlling for AIDS status, the incidence of HIVAN was similar in the 1995–1997 period and the 1989–1994 period (RR, 1.2; 95% CI, 0.8–2.0). However, HIVAN incidence declined significantly in the 1998–2001 period compared to the 1995–1997 period (RR, 0.5; 95% CI, 0.3–0.9).

Fig. 1
Fig. 1
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Figure 2 shows the association of antiretroviral use with subsequent HIVAN incidence. The risk of HIVAN was low in patients who had not developed AIDS, and it is notable that no HIVAN cases developed when HAART was used and AIDS had not occurred (1071 person-years of follow-up). Among individuals with AIDS, lower rates of HIVAN were strongly associated with NRTI use and HAART use, compared with no antiretroviral therapy use (P < 0.001 for trend, Fig. 2).

Fig. 2
Fig. 2
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In a multivariate Poisson regression model African American race (RR, 7.8; 95% CI, 2.5–24.6), the presence of AIDS (RR, 5.0; 95% CI, 2.8–8.7), and antiretroviral treatment status (RR, 0.8; 95% CI, 0.5–1.3 for NRTI compared with no therapy; RR, 0.4; 95% CI, 0.2–0.7 for HAART compared with no therapy) remained significantly associated with HIVAN. Calendar time, injection drug use, and men having sex with men exposure were not significantly associated with HIVAN after adjusting for other variables and were not included in the final model. Similar trends were observed in an analysis including only biopsy-defined HIVAN cases. For example, compared with not using antiretroviral therapy, the RR of HIVAN was 1.1 (95% CI, 0.4–3.3) in those using NRTI therapy, and 0.1 (95% CI, 0.01–0.8) in those using HAART, in a Poisson model adjusting for race and AIDS status.

To evaluate the associations of immunologic factors, virologic factors and HIVAN incidence, CD4 cell count and HIV-1 RNA values were included as time-dependent covariates (updated at 6-month intervals) in a Poisson regression model. Because HIV-1 RNA levels were not available in clinical practice until 1995, this analysis included a subset of 2716 individuals in whom at least one CD4 cell count and one HIV-1 RNA value had been obtained. CD4 cell count was categorized as greater than or less than 200 × 106 cells/l, and HIV-1 RNA was categorized as greater than or less than 100 000 copies/ml. Table 2 shows the associations of proximate CD4 cell count, HIV-1 RNA level and the risk of HIVAN. Compared with having a CD4 cell count ≥ 200 × 106 cells/l, a CD4 cell count < 200 × 106 cells/l was strongly associated with increased HIVAN risk at both low (RR, 3.5; 95% CI, 1.8–7.0) and high HIV-1 RNA levels (RR, 3.0; 95% CI, 1.1–8.7). In contrast, compared with having an HIV-1 RNA < 100 000 copies/ml, having an HIV-1 RNA ≥ 100 000 copies/ml was not significantly associated with HIVAN risk at either high (RR, 2.0; 95% CI, 0.7–6.1) or low CD4 cell counts (RR, 1.7; 95% CI, 0.9–3.2).

Table 2
Table 2
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Discussion

In this first longitudinal study of factors associated with HIVAN incidence, we found a HIVAN rate of approximately 1% per year in African Americans. The presence of AIDS conferred a five-fold increased risk. There was a 50% decline in HIVAN incidence in 1998–2001 compared with 1995–1997. This temporal trend was explained by HAART use, which was associated with a 60% reduction in HIVAN risk. The effect of HAART was most striking in patients with AIDS (Fig. 2), where HIVAN burden was the greatest. However, it is notable that in over 1071 person-years of follow-up no patient developed HIVAN when HAART was initiated prior to the onset of AIDS. The temporal decrease in HIVAN incidence that we observed occurred during a time when the incidence of ESRD was increasing in the general population. For example, in the state of Maryland, the age-, gender- and race-adjusted rate of ESRD in non-diabetics increased from 141 per million in 1991 to 210 per million in 2000 [21], making it very unlikely that the trend we observed was explained by secular trends in kidney disease in the general population.

The nearly exclusive occurrence of HIVAN in African Americans [6] and the strong correlation between HIVAN and advanced HIV-1 disease [7] have been reported by others. A murine model of HIVAN has suggested that expression of HIV-1 regulatory and envelope genes, and not systemic perturbations in cytokine regulation, is sufficient to cause HIVAN [22]. Additionally, renal epithelial cells have been found to be a reservoir for HIV-1, even with the effective use of HAART [13]. Our study strongly suggests that HAART reduces the risk of developing HIVAN in susceptible individuals; however, the mechanism of this effect remains unclear. Our data indicate that a proximate CD4 cell count < 200 × 106 cells/l is a stronger risk factor for HIVAN than a high viral load. This may suggest that the development of HIVAN requires advanced immunosuppression in addition to exposure to viral antigens. A second possibility, which could not be specifically addressed in our cohort, is that low CD4 cell counts are a marker for prolonged duration of HIV infection, which may be the primary risk factor for HIVAN.

The major limitation of our study was that all HIVAN diagnoses were not biopsy confirmed. A broad range of renal pathology has been reported in HIV-1-infected patients with renal disease, including HIVAN, classical focal segmental glomerulosclerosis, acute tubular necrosis, interstitial nephritis, thrombotic micro-angiopathies, and immune complex renal disease [23]. However, as biopsies were not performed in the majority of patients in the cohort with clinically significant renal disease, including only biopsy-proven cases would substantially underestimate the true burden of disease. Our goal in defining clinical criteria for HIVAN, in patients in whom a renal biopsy was not performed, was to design, a reasonable, evidence-based categorization scheme, which could be applied uniformly over time in our clinical cohort. Possible HIVAN cases were identified during prospective cohort data collection, according to sensitive criteria, which were not altered during the 12-year study. We retrospectively adjudicated clinically defined HIVAN cases using a conservative and uniformly applied coding protocol. While misclassifications may have occurred with our clinical coding protocol, such misclassification would tend to bias toward the null hypothesis of no association between HAART use and HIVAN incidence. Patients with clinically defined HIVAN were similar to patients with biopsy-defined disease across a wide range of demographic and clinical variables, including dialysis-free survival time (Table 1). Finally, a statistically significant protective association between HAART and HIVAN incidence was observed in a subgroup analysis including only biopsy-defined HIVAN cases.

Our study implies that the appropriate use of HAART may attenuate the growing epidemic of HIVAN, which disproportionately affects HIV-1-infected patients of African descent. Longer-term follow-up will be needed to determine if renal damage in susceptible individuals is halted or merely slowed by HAART, particularly when control of viremia is incomplete or intermittent. Research is needed to determine whether early markers of glomerular injury [24], family history of renal disease [25], or genetic markers may be used to predict predisposition to HIVAN in HIV-1-infected individuals. As guidelines for HAART initiation have become more conservative [26], identification of increased HIVAN risk may inform decisions about initiation of HAART in individuals with asymptomatic HIV-1 disease.

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Acknowledgements

This research was supported by the National Institute on Drug Abuse (R01-DA11602, K23-DA015616, and K24-DA00432).

Conflict of interest statement: The authors have no conflicts of interest, potential or actual, with the data analysis reported in this manuscript.

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References

1. Rao TKS. Clinical features of human immunodeficiency virus associated nephropathy. Kidney Int 1991, 40(Suppl. 35): S13–S18.

2. Lee H, Manns B, Taub K, Ghali WA, Dean S, Johnson D, et al. Cost analysis of ongoing care of patients with end-stage renal disease: the impact of dialysis modality and dialysis access. Am J Kidney Dis 2002, 40:611–622.

3. Dave MB, Shabih K, Blum S. Maintenance hemodialysis in patients with HIV-associated nephropathy. Clin Nephrol 1998, 50:367–374.

4. Rao TK, Friedman EA, Nicastri AD. The types of renal disease in the acquired immunodeficiency syndrome. N Engl J Med 1987, 316:1062–1068.

5. Ahuja TS, Grady J, Khan S. Changing trends in the survival of dialysis patients with human immunodeficiency virus in the United States. J Am Soc Nephrol 2002, 13:1889–1893.

6. Shahinian V, Rajaraman S, Borucki M, Grady J, Hollander WM, Ahuja TS. Prevalence of HIV-associated nephropathy in autopsies of HIV-infected patients. Am J Kidney Dis 2000, 35: 884–888.

7. Winston JA, Klotman ME, Klotman PE. HIV-associated nephropathy is a late, not early, manifestation of HIV-1 infection. Kidney Int 1999, 55:1036–1040.

8. US Renal Data System (USRDS). USRDS 2000 Annual Data Report. Bethesda, MD: National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health; 2000.

9. UNAIDS. Report on the Global HIV/AIDS Epidemic, July 2002. Available at http://www.unaids.org. Last accessed December 2002.

10. Monahan M, Tanji N, Klotman PE. HIV-associated nephropathy: an urban epidemic. Semin Nephrol 2001, 21:394–402.

11. Wali RK, Drachenberg CI, Papadimitriou JC, Keay S, Ramos E. HIV-1-associated nephropathy and response to highly-active antiretroviral therapy. Lancet 1998, 352:783–784.

12. Szczech LA, Edwards LJ, Sanders LL, van der HC, Bartlett JA, Heald AE, et al. Protease inhibitors are associated with a slowed progression of HIV-related renal diseases. Clin Nephrol 2002, 57:336–341.

13. Winston JA, Bruggeman LA, Ross MD, Jacobson J, Ross L, D'Agati VD, et al. Nephropathy and establishment of a renal reservoir of HIV type 1 during primary infection. N Engl J Med 2001, 344:1979–1984.

14. Cosgrove CJ, Abu-Alfa AK, Perazella MA. Observations on HIV-associated renal disease in the era of highly active antiretroviral therapy. Am J Med Sci 2002, 323:102–106.

15. Eustace JA, Nuermberger E, Choi M, Scheel PJ, Jr., Moore R, Briggs WA. Cohort study of the treatment of severe HIV-associated nephropathy with corticosteroids. Kidney Int 2000, 58:1253–1260.

16. Smith MC, Austen JL, Carey JT, Emancipator SN, Herbener T, Gripshover B, et al. Prednisone improves renal function and proteinuria in human immunodeficiency virus-associated nephropathy. Am J Med 1996, 101:41–48.

17. Burns GC, Paul SK, Toth IR, Sivak SL. Effect of angiotensin-converting enzyme inhibition in HIV-associated nephropathy. J Am Soc Nephrol 1997, 8:1140–1146.

18. Moore RD. Understanding the clinical and economic outcomes of HIV therapy: The Johns Hopkins HIV clinical practice cohort. J Acquir Immune Defic Syndr 1998, 17(suppl. 1):S38–S41.

19. D'Agati V, Appel GB. Renal pathology of human immunodeficiency virus infection. Semin Nephrol 1998, 18:406–421.

20. Centers for Disease Control and Prevention. 1993 Revised classification system for HIV infection and expanded surveillance case definition for AIDS among adolescents and adults. MMWR 1992, 41(RR-17):1–19.

21. U.S. Renal Data System. USRDS 2002 Annual Data Report: Atlas of End-stage-renal Diseases in the United States. Bethesda, MD: National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health; 2002.

22. Bruggeman LA, Dikman S, Meng C, Quaggin SE, Coffman TM, Klotman PE. Nephropathy in human immunodeficiency virus-1 transgenic mice is due to renal transgene expression. J Clin Invest 1997, 100:84–92.

23. Kimmel PL. The nephropathies of HIV infection: pathogenesis and treatment. Curr Opin Nephrol Hypertens 2000, 9:117–122.

24. Szczech LA, Gange SJ, van der HC, Bartlett JA, Young M, Cohen MH, et al. Predictors of proteinuria and renal failure among women with HIV infection. Kidney Int. 2002, 61:195–202.

25. Freedman BI, Soucie JM, Stone SM, Pegram S. Familial clustering of end-stage renal disease in blacks with HIV-associated nephropathy. Am J Kidney Dis 1999, 34:254–258.

26. Department of Health and Human Services and Henry J. Kaiser Family Foundation. Guidelines for the Use of Antiretroviral Agents in HIV-infected Adults and Adolescents. Available at http://www.hivatis.org. Last accessed December 2002.

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Predictors of renal outcome in HIV-associated nephropathy
Post, FA; Campbell, LJ; Hamzah, L; Collins, L; Jones, R; Siwani, R; Johnson, L; Fisher, M; Holt, SG; Bhagani, S; Frankel, AH; Wilkins, E; Ainsworth, JG; Larbalestier, N; Macallan, DC; Banerjee, D; Baily, G; Thuraisingham, RC; Donohoe, P; Hendry, BM; Hilton, RM; Edwards, SG; Hangartner, R; Howie, AJ; Connolly, JO; Easterbrook, PJ
Clinical Infectious Diseases, 46(8): 1282-1289.
10.1086/529385
CrossRef
American Journal of Kidney Diseases
Viral nephropathies: Core curriculum 2008
Berns, JS; Bloom, RD
American Journal of Kidney Diseases, 52(2): 370-381.
10.1053/j.ajkd.2008.01.036
CrossRef
Clinical Infectious Diseases
Kidney Disease in Patients with HIV Infection and AIDS
Winston, J; Deray, G; Hawkins, T; Szczech, L; Wyatt, C; Young, B
Clinical Infectious Diseases, 47(): 1449-1457.
10.1086/593099
CrossRef
Seminars in Nephrology
HIV-Associated Nephropathy: Clinical Presentation, Pathology, and Epidemiology in the Era of Antiretroviral Therapy
Wyatt, CM; Klotman, PE; D'Agati, VD
Seminars in Nephrology, 28(6): 513-522.
10.1016/j.semnephrol.2008.08.005
CrossRef
American Journal of Nephrology
Observations on a cohort of HIV-infected patients undergoing native renal biopsy
Berliner, AR; Fine, DM; Lucas, GM; Rahman, MH; Racusen, LC; Scheel, PJ; Atta, MG
American Journal of Nephrology, 28(3): 478-486.
10.1159/000112851
CrossRef
Journal of the American Society of Nephrology
Urinary NGAL Marks Cystic Disease in HIV-Associated Nephropathy
Paragas, N; Nickolas, TL; Wyatt, C; Forster, CS; Sise, M; Morgello, S; Jagla, B; Buchen, C; Stella, P; Sanna-Cherchi, S; Carnevali, ML; Mattei, S; Bovino, A; Argentiero, L; Magnano, A; Devarajan, P; Schmidt-Ott, KM; Allegri, L; Klotman, P; D'Agati, V; Gharavi, AG; Barasch, J
Journal of the American Society of Nephrology, 20(8): 1687-1692.
10.1681/ASN.2009010065
CrossRef
Hiv Medicine
Prevalence and factors associated with renal impairment in HIV-infected patients, ANRS C03 Aquitaine Cohort, France
Deti, EK; Thiebaut, R; Bonnet, F; Lawson-Ayayi, S; Dupon, M; Neau, D; Pellegrin, JL; Malvy, D; Tchamgoue, S; Dabis, F; Morlat, P
Hiv Medicine, 11(5): 308-317.
10.1111/j.1468-1293.2009.00780.x
CrossRef
Emergency Medicine Clinics of North America
Renal and Urologic Emergencies in the HIV-infected Patient
Liang, SY; Overton, ET
Emergency Medicine Clinics of North America, 28(2): 343-+.
10.1016/j.emc.2010.01.010
CrossRef
AIDS Patient Care and Stds
Prevalence and Factors Associated with Renal Dysfunction Among HIV-Infected Patients
Crum-Cianflone, N; Ganesan, A; Teneza-Mora, N; Riddle, M; Medina, S; Barahona, I; Brodine, S
AIDS Patient Care and Stds, 24(6): 353-360.
10.1089/apc.2009.0326
CrossRef
Nephrology Dialysis Transplantation
Antiretroviral therapy in the treatment of HIV-associated nephropathy
Atta, MG; Gallant, JE; Rahman, MH; Nagajothi, N; Racusen, LC; Scheel, PJ; Fine, DM
Nephrology Dialysis Transplantation, 21(): 2809-2813.
10.1093/ndt/gfl337
CrossRef
Clinical Journal of the American Society of Nephrology
HIV-1 and HIV-associated nephropathy 25 years later
Wyatt, CM; Klotman, PE
Clinical Journal of the American Society of Nephrology, 2(): S20-S24.
10.2215/CJN.03561006
CrossRef
Journal of Pediatrics
Proteinuria in children infected with the human immunodeficiency virus
Chaparro, AI; Mitchell, CD; Abitbol, CL; Wilkinson, JD; Baldarrago, G; Lopez, E; Zilleruelo, G
Journal of Pediatrics, 152(6): 844-849.
10.1016/j.jpeds.2007.11.007
CrossRef
Cochrane Database of Systematic Reviews
Interventions for HIV-associated nephropathy
Yahaya, I; Uthman, AO; Uthman, MMB
Cochrane Database of Systematic Reviews, (4): -.
ARTN CD007183
CrossRef
International Journal of Clinical Practice
Renal complications in HIV
Jones, R; Scott, C; Nelson, M; Levy, J
International Journal of Clinical Practice, 61(6): 991-998.
10.1111/j.1742-1241.2007.01376.x
CrossRef
Mayo Clinic Proceedings
HIV-1 infection and the kidney: An evolving challenge in HIV medicine
De Silva, TI; Post, FA; Griffin, MD; Dockrell, DH
Mayo Clinic Proceedings, 82(9): 1103-1116.

AIDS Patient Care and Stds
Kidney disease in the HIV-infected patient
Fine, DM; Atta, MG
AIDS Patient Care and Stds, 21(): 813-824.
10.1089/apc.2006.0210
CrossRef
Journal of the Formosan Medical Association
Human immunodeficiency virus-associated nephropathy
Lai, CF; Huang, JW; Lin, WC; Hung, CC; Chu, TS
Journal of the Formosan Medical Association, 105(8): 680-684.

Kidney International
Chronic kidney disease as a global public health problem: Approaches and initiatives - a position statement from Kidney Disease Improving Global Outcomes
Levey, AS; Atkins, R; Coresh, J; Cohen, EP; Collins, AJ; Eckardt, KU; Nahas, ME; Jaber, BL; Jadoul, M; Levin, A; Powe, NR; Rossert, J; Wheeler, DC; Lameire, N; Eknoyan, G
Kidney International, 72(3): 247-259.
10.1038/sj.ki.5002343
CrossRef
Clinical Infectious Diseases
Guidelines for the management of chronic kidney disease in HIV-infected patients: Recommendations of the HIV Medicine Association of the Infectious Diseases Society of America
Gupta, SK; Eustace, JA; Winston, JA; Boydstun, II; Ahuja, TS; Rodriguez, RA; Tashima, KT; Roland, M; Franceschini, N; Palella, FJ; Lennox, JL; Klotman, PE; Nachman, SA; Hall, SD; Szczech, LA
Clinical Infectious Diseases, 40(): 1559-1585.

British Journal of Hospital Medicine
HIV and the kidney
Post, FA; Hendry, BM
British Journal of Hospital Medicine, 69(3): 137-140.

Antiviral Therapy
Management of late-presenting patients with HIV infection
Rockstroh, JK; Gatell, J; Landman, R; Antinori, A
Antiviral Therapy, 15(): 25-30.
10.3851/IMP1527
CrossRef
Nature Clinical Practice Nephrology
Interpretation of serologic tests in an HIV-infected patient with kidney disease
Hernandez, GT; Critchfield, JM; Rodriguez, RA
Nature Clinical Practice Nephrology, 2(): 708-712.
10.1038/ncpneph0324
CrossRef
Southern African Journal of Hiv Medicine
HIV infection and the kidney
Fabian, J; Naicker, S
Southern African Journal of Hiv Medicine, (): 12-17.

Nephron Physiology
Changing electrolyte and acido-basic profile in HIV-infected patients in the HAART era
Bagnis, CI; Du Montcel, ST; Fonfrede, M; Jaudon, MC; Thibault, V; Carcelain, G; Valantin, MA; Izzedine, H; Servais, A; Katlama, C; Deray, G
Nephron Physiology, 103(3): 131-138.
10.1159/000092247
CrossRef
AIDS
Chronic kidney disease in HIV infection: an urban epidemic
Wyatt, CM; Winston, JA; Malvestutto, CD; Fishbein, DA; Barash, I; Cohen, AJ; Klotman, ME; Klotman, PE
AIDS, 21(): 2101-2103.

Journal of Infectious Diseases
HIV and the kidney: A spotlight on racial disparities
Wyatt, CM
Journal of Infectious Diseases, 197(): 1490-1492.
10.1086/587995
CrossRef
American Journal of Kidney Diseases
Risk factors for proteinuria in HIV-infected and -uninfected hispanic drug users
Rhee, MS; Schmid, CH; Stevens, L; Forrester, JE
American Journal of Kidney Diseases, 52(4): 683-690.
10.1053/j.ajkd.2008.04.016
CrossRef
Nephrologie & Therapeutique
Kidney diseases in HIV-infected patients
Tourret, J; Tostivint, I; Deray, G; Isnard-Bagnis, C
Nephrologie & Therapeutique, 5(6): 576-591.
10.1016/j.nephro.2009.02.007
CrossRef
Medical Clinics of North America
Racial disparities in the optimal delivery of chronic kidney disease care
Powe, NR; Melamed, ML
Medical Clinics of North America, 89(3): 475-+.
10.1016/j.mcna.2004.11.004
CrossRef
American Journal of Medicine
HIV-associated nephropathy in the era of antiretroviral therapy
Wyatt, CM; Klotman, PE
American Journal of Medicine, 120(6): 488-492.
10.1016/j.amjmed.2007.01.025
CrossRef
American Journal of Kidney Diseases
Kidney biopsy in HIV: Beyond HIV-associated nephropathy
Fine, DM; Perazella, MA; Lucas, GM; Atta, MG
American Journal of Kidney Diseases, 51(3): 504-514.
10.1053/j.ajkd.2007.12.005
CrossRef
Journal of the National Medical Association
Trends in Nephropathy Among HIV-Infected Patients
Buskin, SE; Torno, MS; Talkington, DF; Zhang, M; Jones, JL; Butler, JC; McNaghten, AD; Dworkin, MS
Journal of the National Medical Association, 101(): 1205-1213.

Clinical Journal of the American Society of Nephrology
Outcome and prognosis factors in HIV-infected hemodialysis patients
Tourret, J; Tostivint, I; du Montcel, ST; Bragg-Gresham, J; Karie, S; Vigneau, C; Guiard-Schmid, JB; Deray, G; Bagnis, CI
Clinical Journal of the American Society of Nephrology, 1(6): 1241-1247.
10.2215/CJN.02211205
CrossRef
Journal of Histochemistry & Cytochemistry
APOBEC3G expression is restricted to epithelial cells of the proximal convoluted tubules and is not expressed in the glomeruli of Macaques
Hill, MS; Ruiz, A; Gomez, LM; Miller, JM; Berman, NEJ; Stephens, EB
Journal of Histochemistry & Cytochemistry, 55(1): 63-70.
10.1369/jhc.6A7054.2006
CrossRef
Antiviral Therapy
Does HAART improve renal function? An association between serum cystatin C concentration, HIV viral load and HAART duration
Jaroszewicz, J; Wiercinska-Drapalo, A; Lapinski, TW; Prokopowicz, D; Rogalska, M; Parfieniuk, A
Antiviral Therapy, 11(5): 641-645.

Kidney International
Antiretroviral therapy improves renal function among HIV-infected Ugandans
Peters, PJ; Moore, DM; Mermin, J; Brooks, JT; Downing, R; Were, W; Kigozi, A; Buchacz, K; Weidle, PJ
Kidney International, 74(7): 925-929.
10.1038/ki.2008.305
CrossRef
AIDS Patient Care and Stds
Strategies for initiating combination antiretroviral therapy
Tapper, ML; Daar, ES; Piliero, PJ; Smith, K; Steinhart, C
AIDS Patient Care and Stds, 19(4): 224-238.

Dialysis & Transplantation
Excess burden of end-stage renal disease in blacks: Are we doing enough?
Ifudu, O
Dialysis & Transplantation, 34(): 742-+.

Clinical Infectious Diseases
HIV-associated renal diseases and highly active antiretroviral therapy-induced nephropathy
Roling, J; Schmid, H; Fischereder, M; Draenert, R; Goebel, FD
Clinical Infectious Diseases, 42(): 1488-1495.

Ethnicity & Disease
The Morbidity and Mortality Associated With Kidney Disease in An Hiv-Infected Cohort in Puerto Rico
Mayor, AM; Dworkin, M; Quesada, L; Rios-Olivares, E; Hunter-Mellado, RE
Ethnicity & Disease, 20(1): 163-167.

Clinical Journal of the American Society of Nephrology
Tubulointerstitial Nephropathies in HIV-Infected Patients over the Past 15 Years: A Clinico-Pathological Study
Zaidan, M; Lescure, FX; Brocheriou, I; Dettwiler, S; Guiard-Schmid, JB; Pacanowski, J; Rondeau, E; Pialoux, G; Girard, PM; Ronco, P; Plaisier, E
Clinical Journal of the American Society of Nephrology, 8(6): 930-938.
10.2215/CJN.10051012
CrossRef
Clinical Nephrology
The changing pattern of glomerular disease in HIV and hepatitis C co-infected patients in the era of HAART
Mohan, S; Herlitz, LC; Tan, J; Cheng, JT; Anderson, HL; Stokes, MB; Markowitz, GS; D'Agati, VD; Radhakrishnan, J
Clinical Nephrology, 79(4): 285-291.
10.5414/CN107774
CrossRef
AIDS Research and Human Retroviruses
Antiretroviral-Treated HIV-Infected Women Have Similar Long-Term Kidney Function Trajectories as HIV-Uninfected Women
Estrella, MM; Abraham, AG; Jing, YZ; Parekh, RS; Tien, PC; Merenstein, D; Pearce, CL; Anastos, K; Cohen, MH; Dehovitz, JA; Gange, SJ
AIDS Research and Human Retroviruses, 29(5): 755-760.
10.1089/aid.2012.0248
CrossRef
AIDS
Interruption of antiretroviral therapy is associated with increased plasma cystatin C
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AIDS, 23(1): 71-82.
10.1097/QAD.0b013e32831cc129
PDF (216) | CrossRef
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Relapse of HIV-associated nephropathy after discontinuing highly active antiretroviral therapy
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AIDS, 21(2): 263-264.
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Izzedine, H; Deray, G
AIDS, 21(4): 409-421.
10.1097/QAD.0b013e328011ec40
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AIDS, 22(4): 481-487.
10.1097/QAD.0b013e3282f4706d
PDF (123) | CrossRef
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Longenecker, CT; Scherzer, R; Bacchetti, P; Lewis, CE; Grunfeld, C; Shlipak, MG
AIDS, 23(9): 1089-1096.
10.1097/QAD.0b013e32832a3f24
PDF (152) | CrossRef
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AIDS, 22(14): 1799-1807.
10.1097/QAD.0b013e32830e0152
PDF (291) | CrossRef
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Choi, AI; Shlipak, MG; Hunt, PW; Martin, JN; Deeks, SG
AIDS, 23(16): 2143-2149.
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PDF (317) | CrossRef
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10.1097/QAD.0b013e3283320e12
PDF (314) | CrossRef
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PDF (146) | CrossRef
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Keywords:

HIV-1-associated nephropathy; highly active antiretroviral therapy; HIV-1

© 2004 Lippincott Williams & Wilkins, Inc.

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