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• W2061191788 abstract "HAART-related nephropathies in HIV-infected patients. There is no doubt that highly active antiretroviral therapy (HAART) has been the most important progress in the therapy of human immunodeficiency virus (HIV)-infected patients in the last decade. A growing number of observations suggest that the beneficial effects of HAART also include improvement of HIV-related renal complications. Consequently, the cohort of HIV-infected patients requiring HAART has increased and includes patients with preexisting nephropathies, whether related or unrelated to HIV infection. However, some antiretroviral drugs may have renal- and life-threatening side-effects, especially if underlying renal abnormalities exist. In this review, we focus on those aspects that require particular attention in preventing new health complications in HIV-infected patients. HAART-related nephropathies in HIV-infected patients. There is no doubt that highly active antiretroviral therapy (HAART) has been the most important progress in the therapy of human immunodeficiency virus (HIV)-infected patients in the last decade. A growing number of observations suggest that the beneficial effects of HAART also include improvement of HIV-related renal complications. Consequently, the cohort of HIV-infected patients requiring HAART has increased and includes patients with preexisting nephropathies, whether related or unrelated to HIV infection. However, some antiretroviral drugs may have renal- and life-threatening side-effects, especially if underlying renal abnormalities exist. In this review, we focus on those aspects that require particular attention in preventing new health complications in HIV-infected patients. Current guidelines for treatment of human immunodeficiency virus (HIV) infection recommend the combination of three antiretroviral agents, two reverse transcriptase inhibitors (RTI) plus one protease inhibitor, or the association of three RTIs1.Dybul M. Fauci A.S. Bartlett J.G. et al.Guidelines for using antiretroviral agents among HIV-infected adults and adolescents.Ann Intern Med. 2002; 137: 381-433Crossref PubMed Google Scholar,2.Yeni P.G. Hammer S.M. Carpenter C.C. et al.Antiretroviral treatment for adult HIV infection in 2002: Updated recommendations of the International AIDS Society-USA Panel.JAMA. 2002; 288: 222-235https://doi.org/10.1001/jama.288.2.222Crossref PubMed Scopus (691) Google Scholar. These regimens of highly active antiretroviral therapy (HAART) have dramatically reduced the morbidity and mortality of HIV infection. Nephropathies in HIV-1–infected patients have been recognized for two decades3.Pardo V. Aldana M. Colton R.M. et al.Glomerular lesions in the acquired immunodeficiency syndrome.Ann Intern Med. 1984; 101: 429-434Crossref PubMed Scopus (240) Google Scholar,4.Rao T.K. Filippone E.J. Nicastri A.D. et al.Associated focal and segmental glomerulosclerosis in the acquired immunodeficiency syndrome.N Engl J Med. 1984; 310: 669-673Crossref PubMed Scopus (478) Google Scholar. They consist mostly of glomerular nephropathies, but also of vascular or tubulointerstitial nephropathies5.Weiner N.J. Goodman J.W. Kimmel P.L. The HIV-associated renal diseases: Current insight into pathogenesis and treatment.Kidney Int. 2003; 63: 1618-1631https://doi.org/10.1046/j.1523-1755.2003.00901.xAbstract Full Text Full Text PDF PubMed Scopus (104) Google Scholar. Recently, a growing volume of virologic and histologic evidence suggests that HIV-associated nephropathy (HIVAN), the most usual form of HIV-1–related nephropathy, may be the consequence of HIV-1 replication in the kidney. The possible relation of HIVAN with HIV-1 replication in the kidney correlates with epidemiologic and clinical data showing that HAART may improve HIVAN. However, from a nephrologist's point of view, one consequence of this success has been the emergence of new kidney diseases related to (1) a better control of the HIV infection and (2) the potential nephrotoxicity of antiretroviral therapies. Here we summarize the reported renal adverse effects of the antiretroviral drugs and give some insights into their pathophysiology. We try as well to delineate a new characterization of kidney diseases in HIV-1–infected patients since the beginning of the HAART era. This new profile has been linked to better control of HIV infection and to the potential nephrotoxicity of some antiretroviral treatments. The most common HIV-1–related nephropathy is HIVAN, a focal segmental glomerulosclerosis (FSGS) associated with severe cystic tubular lesions, leading to chronic renal failure, especially in its collapsing variant6.D'Agati V. Suh J.I. Carbone L. et al.Pathology of HIV-associated nephropathy: A detailed morphologic and comparative study.Kidney Int. 1989; 35: 1358-1370Abstract Full Text PDF PubMed Scopus (329) Google Scholar. HIVAN usually affects black patients, and is known to be a leading cause of end-stage renal disease (ESRD) in this population in North America and in Europe7.Cantor E.S. Kimmel P.L. Bosch J.P. Effect of race on expression of acquired immunodeficiency syndrome-associated nephropathy.Arch Intern Med. 1991; 151: 125-128Crossref PubMed Scopus (99) Google Scholar, 8.Nochy D. Glotz D. Dosquet P. et al.Renal disease associated with HIV infection: A multicentric study of 60 patients from Paris hospitals.Nephrol Dial Transplant. 1993; 8: 11-19PubMed Google Scholar, 9.Laradi A. Mallet A. Beaufils H. et al.HIV-associated nephropathy: Outcome and prognosis factors. Groupe d' Etudes Nephrologiques d'Ile de France.J Am Soc Nephrol. 1998; 9: 2327-2335PubMed Google Scholar, 10.Hailemariam S. Walder M. Burger H.R. et al.Renal pathology and premortem clinical presentation of Caucasian patients with AIDS: An autopsy study from the era prior to antiretroviral therapy.Swiss Med Wkly. 2001; 131: 412-417PubMed Google Scholar, 11.Ross M.J. Klotman P.E. Recent progress in HIV-associated nephropathy.J Am Soc Nephrol. 2002; 13: 2997-3004https://doi.org/10.1097/01.ASN.0000040750.40907.99Crossref PubMed Scopus (118) Google Scholar. During the last 5 years, significant advances in the pathophysiology of HIVAN have been achieved. Data from animal models and from human renal biopsies tend to point to HIV-1 infection of renal tubular cells and podocytes as being responsible for the lesions observed in HIVAN (for review, see11.Ross M.J. Klotman P.E. Recent progress in HIV-associated nephropathy.J Am Soc Nephrol. 2002; 13: 2997-3004https://doi.org/10.1097/01.ASN.0000040750.40907.99Crossref PubMed Scopus (118) Google Scholar). Moreover, the recent demonstration that renal tubular cells in patients with HIVAN constitute a viral reservoir where active replication of HIV-1 is independent of that in peripheral blood mononuclear cells strengthens the hypothesis of a direct role of HIV-1 in HIVAN pathogenesis12.Marras D. Bruggeman L.A. Gao F. et al.Replication and compartmentalization of HIV-1 in kidney epithelium of patients with HIV-associated nephropathy.Nat Med. 2002; 8: 522-526https://doi.org/10.1038/nm0502-522Crossref PubMed Scopus (246) Google Scholar. The HIV-1–encoded protein Nef seems to be an important candidate for HIV-1 nephrotoxicity since Nef is capable of inducing podocyte abnormalities in vitro similar to those observed in HIVAN13.Husain M. Gusella G.L. Klotman M.E. et al.HIV-1 Nef induces proliferation and anchorage-independent growth in podocytes.J Am Soc Nephrol. 2002; 13: 1806-1815https://doi.org/10.1097/01.ASN.0000019642.55998.69Crossref PubMed Scopus (129) Google Scholar. Nonetheless, the efficacy of antiretroviral therapy on the course of HIVAN (see below) does not constitute a solid argument for a direct role of HIV-1 in HIVAN as it might well also be related to its indirect effect on systemic HIV-1 replication. In addition, it is not clear if the renal reservoir of HIV-1 thought to be implicated in HIVAN is affected by HAART or not12.Marras D. Bruggeman L.A. Gao F. et al.Replication and compartmentalization of HIV-1 in kidney epithelium of patients with HIV-associated nephropathy.Nat Med. 2002; 8: 522-526https://doi.org/10.1038/nm0502-522Crossref PubMed Scopus (246) Google Scholar. In the pre-HAART era, HIVAN was considered to have a poor prognosis. In addition to the antiretroviral therapy, two types of treatment were proposed to improve the course of HIVAN: prednisone and angiotensin-converting enzyme (ACE) inhibitors. Only one limited prospective study14.Smith M.C. Austen J.L. Carey J.T. et al.Prednisone improves renal function and proteinuria in human immunodeficiency virus-associated nephropathy.Am J Med. 1996; 101: 41-48https://doi.org/10.1016/S0002-9343(96)00065-4Abstract Full Text PDF PubMed Scopus (124) Google Scholar and several retrospective studies15.Eustace J.A. Nuermberger E. Choi M. et al.Cohort study of the treatment of severe HIV-associated nephropathy with corticosteroids.Kidney Int. 2000; 58: 1253-1260https://doi.org/10.1046/j.1523-1755.2000.00280.xAbstract Full Text Full Text PDF PubMed Scopus (113) Google Scholar, 16.Szczech L.A. Edwards L.J. Sanders L.L. et al.Protease inhibitors are associated with a slowed progression of HIV-related renal diseases.Clin Nephrol. 2002; 57: 336-341Crossref PubMed Scopus (99) Google Scholar, 17.Kimmel P.L. Mishkin G.J. Umana W.O. Captopril and renal survival in patients with human immunodeficiency virus nephropathy.Am J Kidney Dis. 1996; 28: 202-208Abstract Full Text PDF PubMed Scopus (136) Google Scholar, 18.Burns G.C. Paul S.K. Toth I.R. et al.Effect of angiotensin-converting enzyme inhibition in HIV-associated nephropathy.J Am Soc Nephrol. 1997; 8: 1140-1146PubMed Google Scholar argue for the use of both corticosteroids and ACE inhibitors in HIVAN. In most studies, however, therapeutic results of ACE inhibitors and prednisone were poor, especially when considering the infectious side-effects of the latter. Antiretroviral therapy such as zidovudine was considered of interest in delaying but not in preventing ESRD19.Cook P.P. Appel R.G. Prolonged clinical improvement in HIV-associated nephropathy with zidovudine therapy.J Am Soc Nephrol. 1990; 1: 842PubMed Google Scholar, 20.Michel C. Dosquet P. Ronco P. et al.Nephropathy associated with infection by human immunodeficiency virus: A report on 11 cases including 6 treated with zidovudine.Nephron. 1992; 62: 434-440Crossref PubMed Scopus (61) Google Scholar, 21.Ifudu O. Rao T.K. Tan C.C. et al.Zidovudine is beneficial in human immunodeficiency virus associated nephropathy.Am J Nephrol. 1995; 15: 217-221Crossref PubMed Scopus (86) Google Scholar. Nonetheless, in the pre-HAART era these reports supported the idea that anti-HIV therapies could be relevant in the therapeutic strategy of HIV-1–related nephropathies17.Kimmel P.L. Mishkin G.J. Umana W.O. Captopril and renal survival in patients with human immunodeficiency virus nephropathy.Am J Kidney Dis. 1996; 28: 202-208Abstract Full Text PDF PubMed Scopus (136) Google Scholar, 19.Cook P.P. Appel R.G. Prolonged clinical improvement in HIV-associated nephropathy with zidovudine therapy.J Am Soc Nephrol. 1990; 1: 842PubMed Google Scholar, 20.Michel C. Dosquet P. Ronco P. et al.Nephropathy associated with infection by human immunodeficiency virus: A report on 11 cases including 6 treated with zidovudine.Nephron. 1992; 62: 434-440Crossref PubMed Scopus (61) Google Scholar, 21.Ifudu O. Rao T.K. Tan C.C. et al.Zidovudine is beneficial in human immunodeficiency virus associated nephropathy.Am J Nephrol. 1995; 15: 217-221Crossref PubMed Scopus (86) Google Scholar. Since the onset of HAART, national epidemiologic data show the reduction of incidence of ESRD due to HIV-associated renal disease in the United States5.Weiner N.J. Goodman J.W. Kimmel P.L. The HIV-associated renal diseases: Current insight into pathogenesis and treatment.Kidney Int. 2003; 63: 1618-1631https://doi.org/10.1046/j.1523-1755.2003.00901.xAbstract Full Text Full Text PDF PubMed Scopus (104) Google Scholar,22.Tokars J.I. Frank M. Alter M.J. et al.National surveillance of dialysis-associated diseases in the United States, 2000.Semin Dial. 2002; 15: 162-171https://doi.org/10.1046/j.1525-139X.2002.00051.xCrossref PubMed Scopus (115) Google Scholar. This suggests that antiretroviral therapy may prevent HIVAN or at least slow its course. Preliminary retrospective series or case reports support the efficacy of HAART in improving outcome in HIVAN16.Szczech L.A. Edwards L.J. Sanders L.L. et al.Protease inhibitors are associated with a slowed progression of HIV-related renal diseases.Clin Nephrol. 2002; 57: 336-341Crossref PubMed Scopus (99) Google Scholar, 23.Wali R.K. Drachenberg C.I. Papadimitriou J.C. et al.HIV-1-associated nephropathy and response to highly-active antiretroviral therapy.Lancet. 1998; 352: 783-784https://doi.org/10.1016/S0140-6736(98)24037-2Abstract Full Text Full Text PDF PubMed Scopus (158) Google Scholar, 24.Winston J.A. Bruggeman L.A. Ross M.D. et al.Nephropathy and establishment of a renal reservoir of HIV type 1 during primary infection.N Engl J Med. 2001; 344: 1979-1984https://doi.org/10.1056/NEJM200106283442604Crossref PubMed Scopus (259) Google Scholar, 25.Saulsbury F. Resolution of organ-specific complications of human immunodeficiency virus infection in children with use of highly active antiretroviral therapy.Clin Infect Dis. 2001; 32: 464-468https://doi.org/10.1086/318493Crossref PubMed Scopus (20) Google Scholar, 26.Cosgrove C.J. Abu-Alfa A.K. Perazella M.A. Observations on HIV-associated renal disease in the era of highly active antiretroviral therapy.Am J Med Sci. 2002; 323: 102-106Abstract Full Text Full Text PDF PubMed Scopus (51) Google Scholar, 27.Kirchner J.T. Resolution of renal failure after initiation of HAART: 3 cases and a discussion of the literature.AIDS Read. 2002; 12: 103-105PubMed Google Scholar. In 1998, Wali et al23.Wali R.K. Drachenberg C.I. Papadimitriou J.C. et al.HIV-1-associated nephropathy and response to highly-active antiretroviral therapy.Lancet. 1998; 352: 783-784https://doi.org/10.1016/S0140-6736(98)24037-2Abstract Full Text Full Text PDF PubMed Scopus (158) Google Scholar reported a 37-year-old HIV-1–positive African American man with HIVAN requiring hemodialysis. A few months after the beginning of HAART, dialysis was stopped, creatinine and proteinuria improved, and histologic lesions recovered. A similar benefit of HAART is reported by Kirchner27.Kirchner J.T. Resolution of renal failure after initiation of HAART: 3 cases and a discussion of the literature.AIDS Read. 2002; 12: 103-105PubMed Google Scholar in two African American patients with suspected HIVAN and in one patient with biopsy-proven HIVAN who exhibited marked improvement in renal function after treatment with two nucleoside RTIs and one antiprotease. In a retrospective cohort study, Szczech et al16.Szczech L.A. Edwards L.J. Sanders L.L. et al.Protease inhibitors are associated with a slowed progression of HIV-related renal diseases.Clin Nephrol. 2002; 57: 336-341Crossref PubMed Scopus (99) Google Scholar reviewed 19 patients with HIVAN or other HIV-1–related renal diseases, leading to ESRD in seven. Treatment with protease inhibitors (and prednisone) was associated with a slower decline in renal function. Cosgrove, Abu-Alfa, and Perazella26.Cosgrove C.J. Abu-Alfa A.K. Perazella M.A. Observations on HIV-associated renal disease in the era of highly active antiretroviral therapy.Am J Med Sci. 2002; 323: 102-106Abstract Full Text Full Text PDF PubMed Scopus (51) Google Scholar reported another retrospective series of 23 patients with HIV-1–related nephropathies, including patients with HIVAN. Thirteen patients, counting those with HIVAN, were treated with HAART and none doubled their serum creatinine. In the non-HAART group, all patients manifested a doubling of serum creatinine, two patients died, and eight required dialysis. One study [abstract; Burckle C et al, J Am Soc Nephrol 13:381A, 2002] retrospectively comparing two cohorts of 102 and 33 patients with biopsy-proven-HIVAN in the pre-HAART and in the HAART era, respectively, also argues for improvement of renal survival by HAART. However, the lack of definitive histologic diagnosis of HIVAN in some of these patients, the absence of controls, the small number of patients and the retrospective design of the studies did not allow firm conclusions to be drawn. Nonetheless, despite the lack of definitive evidence due to the limited true database for HAART efficacy in renal disease, we speculate that combination antiretroviral therapy constitutes the most important therapeutic progress in preventing ESRD in HIV-related nephropathies since the beginning of the HIV epidemic. The idea of prospective controlled trials evaluating HAART on HIVAN or other HIV-1–related nephropathies is not ethically defensible, considering that the clear benefit of HAART on the survival of HIV-infected patients does not allow the design of a placebo-controlled group. The growing population of patients treated with HAART and the predicted larger use of these regimens in patients with previous HIV- or non-HIV–related nephropathies requires the consideration of the potential renal side-effects of antiretroviral treatments. We list below the anti-HIV drugs recognized or reported as potential inducers of renal complications (summarized in Table 1). Some renal abnormalities are only case-reported and concern patients receiving multiple treatments; therefore, their relation with an antiretroviral drug is unclear. The renal toxicity of nonantiretroviral drugs used in HIV patients, such as aminoglycosides, amphotericin B, cidofovir, foscarnet, or pentamidine will not be detailed here.Table 1Renal abnormalities reported in patients with antiretroviral agents used against human immunodeficiency virus (HIV) infectionAntiretroviral subfamilyGeneric name/trade nameRenal abnormalitiesHistologyReferencesProtease inhibitorsAmprenavir/AgeneraseNot reportedIndivavir/CrixivanRenal colic. flank pain, dysuria, acute renal failure, chronic renal failure, leukocyturia, microhematuria, mild proteinuria, urolithiasis, papillary necrosis, crystalluria, urinary tract obstruction by radiolucent calculi, and renal parenchymal defectsTubulointerstitial nephritis with indinavir crystals in tubules28.Kopp J.B. Miller K.D. Mican J.A. et al.Crystalluria and urinary tract abnormalities associated with indinavir.Ann Intern Med. 1997; 127: 119-125Crossref PubMed Scopus (263) Google Scholar, 29.Daudon M. Estepa L. 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Petter A. Romani N. et al.Pyuria in patients treated with indinavir is associated with renal dysfunction.Clin Nephrol. 2000; 54: 261-270PubMed Google Scholar, 41.Dieleman J.P. Sturkenboom M.C. Jambroes M. et al.Risk factors for urological symptoms in a cohort of users of the HIV protease inhibitor indinavir sulfate: The ATHENA cohort.Arch Intern Med. 2002; 162: 1493-1501https://doi.org/10.1001/archinte.162.13.1493Crossref PubMed Scopus (42) Google Scholar, 42.Meraviglia P. Angeli E. Del Sorbo F. et al.Risk factors for indinavir-related renal colic in HIV patients: Predictive value of indinavir dose/body mass index.Aids. 2002; 16: 2089-2093https://doi.org/10.1097/00002030-200210180-00019Crossref PubMed Scopus (20) Google Scholar, 43.Voigt E. Wickesberg A. 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Yum M.N. et al.Acute tubulointerstitial nephritis attributable to indinavir therapy.Am J Kidney Dis. 2000; 35: E16Abstract Full Text Full Text PDF PubMed Google Scholar, 93.Dieleman J.P. Van Der Feltz M. Bangma C.H. et al.Papillary necrosis associated with the HIV protease inhibitor indinavir.Infection. 2001; 29: 232-233https://doi.org/10.1007/s15010-001-1105-yCrossref PubMed Scopus (18) Google ScholarLopinavir (plus ritonavir)/KaletraNot reportedNelfinavir/ViraceptRenal colic48.Engeler D.S. John H. Rentsch K.M. et al.Nelfinavir urinary stones.J Urol. 2002; 167: 1384-1385https://doi.org/10.1097/00005392-200203000-00042Crossref PubMed Google ScholarRitonavir/NorvirAcute renal failure49.Duong M. Sgro C. Grappin M. et al.Renal failure after treatment with ritonavir.Lancet. 1996; 348: 693Abstract Full Text Full Text PDF PubMed Scopus (43) Google Scholar, 51.Witzke O. Plentz A. 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Renal tubular acidosis and hypophosphataemia after treatment with nucleoside reverse transcriptase inhibitors.Aids. 2001; 15: 140-141https://doi.org/10.1097/00002030-200101050-00027Crossref PubMed Scopus (37) Google ScholarZalcitabine/HividNot reportedZidovudine (azidothymidine)/RetrovirNot reportedNucleotide reverse transcriptase inhibitorsTenofovir disoproxil fumarate/VireadAcute renal failure, proximal tubular dysfunction (Fanconi's syndrome), nephrogenic diabetes insipidus, nephritic syndrome, leucocyturia of apparent tubular originProximal tubular cells abnormalities71.Verhelst D. Monge M. Meynard J.L. et al.Fanconi syndrome and renal failure induced by tenofovir: A first case report.Am J Kidney Dis. 2002; 40: 1331-1333https://doi.org/10.1053/ajkd.2002.36924Abstract Full Text Full Text PDF PubMed Scopus (297) Google Scholar, 72.Coca S. 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O'Hearn M. et al.Enfuvirtide, an HIV-1 fusion inhibitor, for drug-resistant HIV infection in North and South America.N Engl J Med. 2003; 348: 2175-2185https://doi.org/10.1056/NEJMoa035026Crossref PubMed Scopus (791) Google Scholar Open table in a new tab Among protease inhibitors, indinavir is the most frequently associated with renal or urologic side-effects: reversible acute renal failure, chronic renal failure, leukocyturia, microhematuria, mild proteinuria, nephrolithiasis, papillary necrosis, and crystalluria Table 1. Symptoms may occur as early as 1 week following initiation of indinavir therapy28.Kopp J.B. Miller K.D. Mican J.A. et al.Crystalluria and urinary tract abnormalities associated with indinavir.Ann Intern Med. 1997; 127: 119-125Crossref PubMed Scopus (263) Google Scholar. They are related to the crystallization of indinavir that can occur in all anatomic structures from the proximal tubules to the bladder. Infrared spectrophotometry, mass spectrometry and high-performance liquid chromatography (HPLC) studies have confirmed that these crystals are composed of indinavir28.Kopp J.B. Miller K.D. Mican J.A. et al.Crystalluria and urinary tract abnormalities associated with indinavir.Ann Intern Med. 1997; 127: 119-125Crossref PubMed Scopus (263) Google Scholar,29.Daudon M. Estepa L. Viard J.P. et al.Urinary stones in HIV-1-positive patients treated with indinavir.Lancet. 1997; 349: 1294-1295Abstract Full Text Full Text PDF PubMed Scopus (121) Google Scholar. Risk factors are urine pH above 6, high dose of indinavir, besides the usual risk factors for nephrolithiasis (dehydration, warm environmental temperature, etc.)29.Daudon M. Estepa L. Viard J.P. et al.Urinary stones in HIV-1-positive patients treated with indinavir.Lancet. 1997; 349: 1294-1295Abstract Full Text Full Text PDF PubMed Scopus (121) Google Scholar, 30.Dieleman J.P. Gyssens I.C. 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