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  • Review Article
  • Published:

HIV-associated immune complex kidney disease

Nature Reviews Nephrology volume 12, pages 291–300 (2016)Cite this article

Subjects

Key Points

  • HIV infection is associated with numerous adverse renal manifestations, including HIV-associated nephropathy (HIVAN), HIV-associated immune complex kidney disease (HIVICD), and other glomerulonephritides

  • Renal biopsy in patients infected with HIV is essential to differentiate HIVICD from other forms of HIV-associated kidney diseases, such as HIVAN or nephrotoxicity

  • The development of HIVICD is the result of the complex interplay between host–pathogen interactions, genetic susceptibility, and environmental factors

  • Data regarding the optimal treatment strategy for patients with HIVICD are limited

Abstract

The introduction in the late 20th century of combination antiretroviral therapy (cART) to treat patients infected with HIV has changed the natural history of the disease from an acute illness that rapidly culminates in death, to a chronic condition that can be managed with medications. Over the past decade the epidemiology of kidney disease in US patients infected with HIV has changed, perhaps because of the increased availability and use of cART. Patients with HIV infection exhibit unique immunologic characteristics, including immunodeficiency and dysregulation of immunoglobulin synthetic responses and T-cell function, which can result in glomerular immune complex deposition and subsequent kidney injury. This Review examines the differential diagnoses of HIV-associated immune complex kidney diseases (HIVICD), and discusses the clinical manifestations and mechanisms underlying their development. We address the issues associated with treatment, clinical outcomes, and research needs to enhance our ability to diagnose and optimally treat patients with HIVICD.

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Figure 1: Light microscopic features of various HIV immune complex diseases.
Figure 2: Theoretical interplay between host factors, environmental factors, genetic susceptibility, and factors associated with viral infection, in immune complex renal disease.
Figure 3: Ouchterlony diffusion plate analysis.

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References

  1. Fernando, S. K., Finkelstein, F. O., Moore, B. A. & Weissman, S. Prevalence of chronic kidney disease in an urban HIV infected population. Am. J. Med. Sci. 335, 89–94 (2008).

    Article  PubMed  Google Scholar 

  2. Szczech, L. A. et al. Predictors of proteinuria and renal failure among women with HIV infection. Kidney Int. 61, 195–202 (2002).

    Article  PubMed  Google Scholar 

  3. Rao, T. K. et al. Associated focal and segmental glomerulosclerosis in the acquired immunodeficiency syndrome. N. Engl. J. Med. 310, 669–673 (1984).

    Article  CAS  PubMed  Google Scholar 

  4. Pardo, V. et al. Glomerular lesions in the acquired immunodeficiency syndrome. Ann. Intern. Med. 101, 429–434 (1984).

    Article  CAS  PubMed  Google Scholar 

  5. Rosenberg, A. Z., Naicker, S., Winkler, C. A. & Kopp, J. B. HIV-associated nephropathies: epidemiology, pathology, mechanisms and treatment. Nat. Rev. Nephrol. 10, 150–160 (2015).

    Article  CAS  Google Scholar 

  6. Benveniste, O. et al. Two episodes of acute renal failure, rhabdomyolysis, and severe hepatitis in an AIDS patient successively treated with ritonavir and indinavir. Clin. Infect. Dis. 28, 1180–1181 (1999).

    Article  CAS  PubMed  Google Scholar 

  7. Rao, T. K. Acute renal failure in human immunodeficiency virus infection. Semin. Nephrol. 18, 378–395 (1998).

    CAS  PubMed  Google Scholar 

  8. Kopp, J. B. et al. Crystalluria and urinary tract abnormalities associated with indinavir. Ann. Intern. Med. 128, 118–125 (1997).

    Google Scholar 

  9. Kopp, J. B. et al. Indinavir-associated interstitial nephritis and urothelial inflammation: clinical and cytologic findings. Clin. Infect. Dis. 34, 1122–1128 (2002).

    Article  CAS  PubMed  Google Scholar 

  10. Olyaei, A. J., deMattos, A. M. & Bennett, W. M. Renal toxicity of protease inhibitors. Curr. Opin. Nephrol. Hypertens. 9, 473–476 (2000).

    Article  CAS  PubMed  Google Scholar 

  11. Reiter, W. J., Schön-Pernerstorfer, H., Dorfinger, K., Hofbauer, J. & Marberger, M. Frequency of urolithiasis in individuals seropositive for human immunodeficiency virus treated with indinavir is higher than previously assumed. J. Urol. 161, 1082–1084 (1999).

    Article  CAS  PubMed  Google Scholar 

  12. Kohan, A. D., Armenakas, N. A. & Fracchia, J. A. Indinavir urolithiasis: an emerging cause of renal colic in patients with human immunodeficiency virus. J. Urol. 161, 1765–1768 (1999).

    Article  CAS  PubMed  Google Scholar 

  13. Rao, T. K. Renal complications in HIV disease. Med. Clin. North Am. 80, 1437–1451 (1996).

    Article  CAS  PubMed  Google Scholar 

  14. Wearne, N., Swanepoel, C. R., Boulle, A., Duffield, M. S. & Rayner, B. L. The spectrum of renal histologies seen in HIV with outcomes, prognostic indicators and clinical correlations. Nephrol. Dial. Transplant. 27, 4109–4101 (2012).

    Article  PubMed  Google Scholar 

  15. Foy, M. C. et al. Comparison of risk factors and outcomes in HIV immune complex kidney disease and HIV-associated nephropathy. Clin. J. Am. Soc. Nephrol. 8, 1524–1532 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  16. Weiner, N. J., Goodman, J. W. & Kimmel, P. L. The HIV-associated renal diseases: current insight into pathogenesis and treatment. Kidney Int. 63, 1618–1631 (2003).

    Article  PubMed  Google Scholar 

  17. Kimmel, P. L., Barisoni, L. & Kopp, J. B. Pathogenesis and treatment of HIV-associated renal diseases: lessons from clinical and animal studies, molecular pathologic correlations, and genetic investigations. Ann. Intern. Med. 139, 214–226 (2003).

    Article  CAS  PubMed  Google Scholar 

  18. Rachakonda, A. K. & Kimmel, P. L. CKD in HIV-infected patients other than HIV-associated nephropathy. Adv. Chron. Kidney. Dis. 17, 83–93 (2010).

    Article  Google Scholar 

  19. Cohen, S. D. & Kimmel, P. L. Immune complex renal disease and human immunodeficiency virus infection. Semin. Nephrol. 28, 535–544 (2008).

    Article  PubMed  Google Scholar 

  20. Kimmel, P. L. et al. Brief report: idiotypic IgA nephropathy in patients with human immunodeficiency virus infection. N. Engl. J. Med. 327, 729–730 (1992).

    Article  Google Scholar 

  21. Kimmel, P. L. et al. HIV-associated immune-mediated renal disease. Kidney Int. 44, 1327–1340 (1993).

    Article  CAS  PubMed  Google Scholar 

  22. Stokes, M. B. et al. Immune complex glomerulonephritis in patients co-infected with HIV and hepatitis C virus. Am. J. Kidney Dis. 29, 514–525 (1997).

    Article  CAS  PubMed  Google Scholar 

  23. Haas, M., Kaul, S. & Eustace, J. A. HIV-associated immune complex glomerulonephritis with 'lupus-like' features: a clinicopathologic study of 14 cases. Kidney Int. 67, 1381–1390 (2005).

    Article  PubMed  Google Scholar 

  24. Nochy, D. et al. Renal disease associated with HIV infection: a multicentric study of 60 patients from Paris hospitals. Nephrol. Dial. Transplant. 8, 11–19 (1993).

    Article  CAS  PubMed  Google Scholar 

  25. Szczech, L. A. et al. The clinical epidemiology and course of the spectrum of renal diseases associated with HIV infection. Kidney Int. 66, 1145–1152 (2004).

    Article  PubMed  Google Scholar 

  26. Schectman, J. M. & Kimmel, P. L. Remission of hepatitis-B associated membranous glomerulonephritis in human immunodeficiency virus infection. Am. J. Kidney Dis. 17, 716–718 (1991).

    Article  CAS  PubMed  Google Scholar 

  27. Kimmel, P. L., Abraham, A. A. & Phillips, T. M. Membranoproliferative glomerulonephritis in a patient treated with interferon-alpha for human immunodeficiency virus infection. Am. J. Kidney Dis. 24, 858–863 (1994).

    Article  CAS  PubMed  Google Scholar 

  28. Praditpornsilpa, K. et al. Renal pathology and HIV infection in Thailand. Am. J. Kidney Dis. 33, 282–286 (1999).

    Article  CAS  PubMed  Google Scholar 

  29. Williams, D. I. et al. Presentation, pathology, and outcome of HIV-associated renal disease in a specialist centre for HIV/AIDS. Sex. Transm. Infect. 74, 179–184 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Cohen, S. D. & Kimmel, P. L. Renal biopsy is necessary for the diagnosis of HIV-associated renal diseases. Nat. Clin. Pract. Nephrol. 5, 22–23 (2009).

    Article  PubMed  Google Scholar 

  31. Barbiano di Belgiojoso, G. et al. Immunotactoid glomerulopathy in a HIV-infected patient: a novel association. Nephrol. Dial. Transplant. 11, 857–859 (1996).

    Article  Google Scholar 

  32. Naggie, S. & Hicks, C. Protease inhibitor-based antiretroviral therapy in treatment-naive HIV-1-infected patients: the evidence behind the options. J. Antimicrob. Chemother. 6, 1094–1099 (2010).

    Article  CAS  Google Scholar 

  33. Rao, T. K., Friedman, E. A. & Nicastri, A. D. The types of renal disease in the acquired immunodeficiency syndrome. N. Engl. J. Med. 316, 1062–1068 (1987).

    Article  CAS  PubMed  Google Scholar 

  34. Genovese, G. et al. Association of trypanolytic ApoL1 variants with kidney disease in African Americans. Science 329, 841–845 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Kopp, J. B. et al. APOL1 genetic variants in focal segmental glomerulosclerosis and HIV-associated nephropathy. J. Am. Soc. Nephrol. 22, 2129–2137 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Freedman, B. I. et al. The apolipoprotein L1 (APOL1) gene and nondiabetic nephropathy in African Americans. J. Am. Soc. Nephrol. 21, 1422–1426 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Thomson, R. et al. Evolution of the primate trypanolytic factor APOL1. Proc. Natl Acad. Sci. USA 111, E2130–E2139 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Udler, M. S. et al. Effect of genetic African ancestry on eGFR and kidney disease. J. Am. Soc. Nephrol. 26, 1682–1692 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Fine, D. M. et al. APOL1 risk variants predict histopathology and progression to ESRD in HIV-related kidney disease. J. Am. Soc. Nephrol. 23, 343–350 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Matovu, E. et al. Enabling the genomic revolution in Africa. Science 344, 1346–1348 (2014).

    Article  PubMed  Google Scholar 

  41. D'Agati, V., Suh, J. I., Carbone, L., Cheng, J. T. & Appel, G. Pathology of HIV-associated nephropathy: a detailed morphologic and comparative study. Kidney Int. 35, 1358–1370 (1989).

    Article  CAS  PubMed  Google Scholar 

  42. Kimmel, P. L., Ferreira-Centeno, A., Farkas-Szallasi, T., Abraham, A. A. & Garrett, C. T. Viral DNA in microdissected renal biopsy tissue from HIV infected patients with nephrotic syndrome. Kidney Int. 43, 1347–1352 (1993).

    Article  CAS  PubMed  Google Scholar 

  43. Cohen, S. D. & Kimmel, P. L. HIV-associated renal diseases in Africa: a desperate need for additional study. Nephrol. Dial. Transplant. 22, 2116–2119 (2007).

    Article  PubMed  Google Scholar 

  44. Emem, C. P. et al. Renal disease in HIV-seropositive patients in Nigeria: an assessment of prevalence, clinical features, and risk factors. Nephrol. Dial. Transplant. 23, 741–746 (2008).

    Article  PubMed  Google Scholar 

  45. Mallipattu, S. K., Salem, F. & Wyatt, C. M. The changing epidemiology of HIV-related chronic kidney disease in the era of antiretroviral therapy. Kidney Int. 86, 259–265 (2014).

    Article  PubMed  Google Scholar 

  46. Gerntholtz, T. E., Goetsch, S. J. & Katz, I. HIV-related nephropathy: a South African perspective. Kidney Int. 69, 1885–1991 (2006).

    Article  CAS  PubMed  Google Scholar 

  47. Han, T. M., Naicker, S., Ramdial, P. K. & Assounga, A. G. A cross-sectional study of HIV-seropositive patients with varying degrees of proteinuria in South Africa. Kidney Int. 69, 2243–2250 (2006).

    Article  CAS  PubMed  Google Scholar 

  48. Casanova, S. et al. Pattern of glomerular involvement in human immunodeficiency virus-infected patients: an Italian study. Am. J. Kidney Dis. 26, 446–453 (1995).

    Article  CAS  PubMed  Google Scholar 

  49. Gupta, V. et al. HIV associated renal disease: a pilot study from North India. Indian J. Med. Res. 137, 950–956 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Glassock, R. J. Immune complex-induced glomerular injury in viral diseases: an overview. Kidney Int. Suppl. 35, S5–S7 (1991).

    CAS  PubMed  Google Scholar 

  51. Killen, P. D., Melcion, C., Bonadio, J. F., Morel-Maroger, L. & Striker, G. E. Glomerular response to immunologic injury, studies on progression. Springer Semin. Immunopathol. 5, 297–320 (1982).

    Article  CAS  PubMed  Google Scholar 

  52. Couser, W. G. & Johnson, R. J. The etiology of glomerulonephritis: roles of infection and autoimmunity. Kidney Int. 86, 905–914 (2014).

    Article  CAS  PubMed  Google Scholar 

  53. Kimmel, P. L. & Phillips, T. M. in Renal and Urologic Aspects of HIV Infection (eds Kimmel, P. L. et al.) 77–110 (Churchill Livingstone, 1995).

    Google Scholar 

  54. Couser, W. G. Basic and translational concepts of immune-mediated glomerular diseases. J. Am. Soc. Nephrol. 23, 381–399 (2012).

    Article  CAS  PubMed  Google Scholar 

  55. Wilson, C. B. & Dixon, F. J. in The Kidney (eds Brenner, B. M. & Rector, F. C. Jr) 838–940 (Saunders, 1976).

    Google Scholar 

  56. Theophilopoulos, A. N. & Dixon, F. J. Immune complexes in human diseases. Am. J. Pathol. 100, 529–594 (1980).

    Google Scholar 

  57. Navalkar, R. G., Norlin, M. & Ouchterlony, O. Characterization of leprosy sera with various mycobacterial antigens using double diffusion-in-gel analysis. Int. Arch. Allergy Appl. Immunol. 25, 105–113 (1964).

    Article  CAS  PubMed  Google Scholar 

  58. Woodroffe, A. J. & Wilson, C. B. An evaluation of elution techniques in the study of immune complex glomerulonephritis. J. Immunol. 118, 1788–1794 (1977).

    CAS  PubMed  Google Scholar 

  59. Kiryluk, K. & Novak, J. The genetics and immunopathology of IgA nephropathy. J. Clin. Invest. 124, 2325–2332 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Wyatt, R. J. & Julian, B. A. IgA nephropathy. N. Engl. J. Med. 368, 2402–2414 (2013).

    Article  CAS  PubMed  Google Scholar 

  61. Johnson, R. J. et al. Membranoproliferative glomerulonephritis associated with hepatitis C virus infection. N. Engl. J. Med. 328, 456–470 (1993).

    Article  Google Scholar 

  62. Nishanian, P., Huskins, K. R., Stehn, S., Detels, R. & Fahey, J. L. A simple method for improved assay demonstrates that HIV p24 antigen is present as immune complexes in most sera from HIV-infected individuals. J. Infect. Dis. 162, 21–28 (1990).

    Article  CAS  PubMed  Google Scholar 

  63. Portera, M. et al. Free and antibody-complexed antigen and antibody profile in apparently healthy HIV seropositive individuals and in AIDS patients. J. Med. Virol. 30, 30–35 (1990).

    Article  CAS  PubMed  Google Scholar 

  64. Carini, C. et al. Characterization of specific immune complexes in HIV-related disorders. Scand. J. Immunol. 26, 21–28 (1987).

    Article  CAS  PubMed  Google Scholar 

  65. McDougal, J. S. et al. Antibody response to human immunodeficiency virus in homosexual men. Relation of antibody specificity, titer, and isotype to clinical status, severity of immunodeficiency and disease progression. J. Clin. Invest. 80, 316–324 (1987).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Ellaurie, M., Calvelli, T. & Rubinstein, A. Immune complexes in pediatric human immunodefiency virus infection. Am. J. Dis. Child. 144, 1207–1209 (1990).

    CAS  PubMed  Google Scholar 

  67. Szczech, L. A. et al. The uncertain significance of anti-glomerular basement membrane antibody among HIV-infected persons with kidney disease. Am. J. Kidney Dis. 48, E55–E59 (2006).

    Article  PubMed  Google Scholar 

  68. Kimmel, P. L. in Immunologic Renal Diseases 2nd edn (eds Nielson, E. G. & Couser, W. G.) 1203–1223 (Lippincott Williams and Wilkins, 2001).

    Google Scholar 

  69. Shen, X. & Tomaras, G. D. Alterations of the B-cell response by HIV-1 replication. Curr. HIV/AIDS Rep. 8, 23–30 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Lane, H. C. et al. Abnormalities of B-cell activation and immunoregulation in patients with the acquired immunodeficiency syndrome. N. Engl. J. Med. 309, 453–458 (1983).

    Article  CAS  PubMed  Google Scholar 

  71. Michael, A. F. Jr, Drummond, K. N., Good, R. A. & Vernier, R. L. Acute poststreptococcal glomerulonephritis: immune complex disease. J. Clin. Invest. 45, 237–248 (1966).

    Article  PubMed  PubMed Central  Google Scholar 

  72. Treser, G. et al. Partial characterization of antigenic streptococcal plasma membrane components in acute glomerulonehritis. J. Clin. Invest. 49, 762–768 (1970).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Nissenson, A. R., Baraff, L. J., Fine, R. N. & Knutson, D. W. Poststreptococcal acute glomerulonephritis: facts and controversy. Ann. Intern. Med. 91, 76–86 (1979).

    Article  CAS  PubMed  Google Scholar 

  74. Gamble, C. N. & Rearsdan, J. B. Immunopathogenesis of syphilitic glomerulonephritis. N. Engl. J. Med. 292, 449–454 (1975).

    Article  CAS  PubMed  Google Scholar 

  75. Gorevic, P. D. et al. Mixed cryoglobulinemia: clinical aspects and long-term follow-up of 40 patients. Am. J. Med. 69, 287–306 (1980).

    Article  CAS  PubMed  Google Scholar 

  76. Fabrizi, F. Hepatitis C virus, cryoglobulinemia, and kidney: novel evidence. Scientifica 2012, 128382 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  77. Ward, P. A. & Kibukamusoke, J. W. Evidence for soluble immune complexes in the pathogenesis of quartan malaria. Lancet 293, 283–285 (1969).

    Article  Google Scholar 

  78. Korbet, S. M. & Schwartz, M. M. Human immunodeficiency virus infection and nephrotic syndrome. Am. J. Kidney Dis. 20, 97–103 (1992).

    Article  CAS  PubMed  Google Scholar 

  79. Bodi, I., Abraham, A. A. & Kimmel, P. L. Macrophages in HIV-associated kidney diseases. Am. J. Kidney Dis. 24, 762–767 (1994).

    Article  CAS  PubMed  Google Scholar 

  80. Ross, M. J. Advances in the pathogenesis of HIV-associated kidney diseases. Kidney Int. 86, 266–274 (2014).

    Article  CAS  PubMed  Google Scholar 

  81. Katz, A. et al. IgA nephritis in HIV-positive patients: a new HIV-associated nephropathy? Clin. Nephrol. 38, 61–68 (1992).

    CAS  PubMed  Google Scholar 

  82. Kajiyama, W., Kopp, J. B., Marinos, N. J., Klotman, P. E. & Dickie, P. Glomerulosclerosis and viral gene expression in HIV-transgenic mice: role of nef. Kidney Int. 58, 1148–1159 (2000).

    Article  CAS  PubMed  Google Scholar 

  83. Mikulak, J. & Singhal, P. C. HIV-1 and kidney cells: better understanding of viral interaction. Nephron Exp. Nephrol. 115, e15–e21 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  84. Bruggeman, L. A. Insight versus quagmire with compound HIV transgenics. J. Am. Soc. Nephrol. 10, 2085–2086 (2009).

    Article  Google Scholar 

  85. Tishon, A., Salmi, A., Ahmed, R. & Oldstone, M. B. Role of viral strains and host genes in determining levels of immune complexes in a model system: implications for HIV infection. AIDS Res. Hum. Retroviruses 7, 963–969 (1991).

    Article  CAS  PubMed  Google Scholar 

  86. Stephens, E. B., Tian, C., Dalton, S. B. & Gattone, V. H. 2nd Simian-human immune deficiency virus-associated nephropathy in macaques. AIDS Res. Hum. Retroviruses 16, 1295–1306 (2000).

    Article  CAS  PubMed  Google Scholar 

  87. Liu, Z.Q. et al. Derivation and biological characterization of a molecular clone of SHIV (KU-2) that causes AIDS, neurological disease, and renal disease in rhesus macaques. Virology 260, 295–307 (1999).

    Article  CAS  PubMed  Google Scholar 

  88. Alpers, C. E. et al. Focal segmental glomerulosclerosis in primates infected with a simian immunodeficiency virus. AIDS Res. Hum. Retroviruses 13, 413–424 (1997).

    Article  CAS  PubMed  Google Scholar 

  89. Strauss, J. et al. Renal disease in children with the acquired immunodeficiency syndrome. N. Engl. J. Med. 321, 625–630 (1989).

    Article  CAS  PubMed  Google Scholar 

  90. McCulloch, M. I. & Ray, P. E. Kidney disease in HIV-positive children. Sem. Nephrol. 28, 585–594 (2008).

    Article  Google Scholar 

  91. D'Agati, V. & Appel, G. B. HIV infection and the kidney. J. Am. Soc. Nephrol. 8, 138–152 (1997).

    Article  CAS  PubMed  Google Scholar 

  92. Cohen, A. H. & Nast, C. C. HIV-associated nephropathy. A unique combined glomerular, tubular, and interstitial lesion. Mod. Pathol. 1, 87–97 (1988).

    CAS  PubMed  Google Scholar 

  93. Lee, C. J. et al. The clinicopathologic significance of endothelial tubuloreticular inclusions in glomerular diseases. Ultrastruct. Pathol. 37, 386–394 (2013).

    Article  PubMed  Google Scholar 

  94. Markowitz, G. S., Nasr, S. H., Stokes, M. B. & D'Agati, V. D. Treatment with IFN-α, -β, or -γ is associated with collapsing focal segmental glomerulosclerosis. Clin. J. Am. Soc. Nephrol. 5, 607–615 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Orenstein, J. M., Preble, O. T., Kind, P. & Schulof, R. The relationship of serum alpha-interferon and ultrastructural markers in HIV-seropositive individuals. Ultrastruct. Pathol. 11, 673–679 (1987).

    Article  CAS  PubMed  Google Scholar 

  96. Nebuloni, M. et al. Glomerular lesions in HIV-positive patients: a 20-year biopsy experience from Northern Italy. Clin. Nephrol. 72, 38–45 (2009).

    Article  CAS  PubMed  Google Scholar 

  97. Nasr, S. H., Radhakrishnan, J. & D'Agati, V. D. Bacterial infection-related glomerulonephritis in adults. Kidney Int. 83, 792–803 (2013).

    Article  CAS  PubMed  Google Scholar 

  98. Nissenson, A. R., Baraff, L. J., Fine, R. N. & Knutson, D. W. Poststreptococcal acute glomerulonephritis: fact and controversy. Ann. Intern. Med. 91, 76–86 (1979).

    Article  CAS  PubMed  Google Scholar 

  99. Balow, J. E. Nephropathy in the context of HIV infection. Kidney Int. 67, 1632–1633 (2005).

    Article  PubMed  Google Scholar 

  100. Johnson, R. J. & Couser, W. G. Hepatitis B infection and renal disease: clinical immunopathogenetic and therapeutic considerations. Kidney Int. 37, 663–676 (1990).

    Article  CAS  PubMed  Google Scholar 

  101. Meyers, C. M., Seef, L. B., Stehman-Breen, C. O. & Hoofnagle, J. H. Hepatitis C and renal disease: an update. Am. J. Kidney Dis. 42, 631–657 (2003).

    Article  PubMed  Google Scholar 

  102. Sethi, S. & Fervenza, F. C. Membranoproliferative glomerulonephritis — a new look at an old entity. N. Engl. J. Med. 366, 1119–1113 (2012).

    Article  CAS  PubMed  Google Scholar 

  103. Beck, L. H. et al. M-type phospholipase A2 receptor as target antigen in idiopathic membranous nephropathy. N. Eng. J. Med. 361, 11–21 (2009).

    Article  CAS  Google Scholar 

  104. Alarcon-Zurita, A. et al. Membranous glomerulonephritis with nephrotic syndrome in a HIV positive patient-remarkable remission with triple therapy. Nephrol. Dial. Transplant. 15, 1097–1098 (2000).

    Article  CAS  PubMed  Google Scholar 

  105. Lai, K. N. et al. Membranous nephropathy related to hepatitis B virus in adults. N. Engl. J. Med. 324, 1457–1463 (1991).

    Article  CAS  PubMed  Google Scholar 

  106. Stehman-Breen, C., Alpers, C. E., Couser, W. G., Willson, R. & Johnson, R. J. Hepatitis C virus associated membranous glomerulonephritis. Clin. Nephrol. 44, 141–147 (1995).

    CAS  PubMed  Google Scholar 

  107. George, E. et al. The impact of hepatitis C coinfection on kidney disease related to human immunodeficiency virus (HIV): a biopsy study. Medicine (Baltimore) 90, 289–295 (2011).

    Article  CAS  Google Scholar 

  108. Scotto, G. et al. Cryoglobulinemia in subjects with HCV infection alone, HIV infection, and HCV/HIV coinfection. J. Infect. 52, 294–299 (2006).

    Article  CAS  PubMed  Google Scholar 

  109. Dimitrakopoulos, A., Kordossis, T., Hatzakis, A. & Moutsopoulos, H. M. Mixed cryoglobulinemia in HIV-1 infection: the role of HIV-1. Ann. Intern. Med. 130, 226–230 (1999).

    Article  CAS  PubMed  Google Scholar 

  110. Haas, M., Rajaraman, S., Ahuja, T., Kittaka, M. & Cavallo, T. Fibrillary/immunotactoid glomerulonephritis in HIV-positive patients: a report of three cases. Nephrol. Dial. Transplant. 15, 1679–1683 (2000).

    Article  CAS  PubMed  Google Scholar 

  111. Martin, J. L., Thomas, D. & Colindres, R. E. Immunotactoid glomerulopathy in an HIV-positive African-American man. Am. J. Kidney Dis. 42, E6–E10 (2003).

    Article  PubMed  Google Scholar 

  112. Alpers, C. E. & Kowalewska, J. Fibrillary glomerulonephritis and immunotactoid glomerulopathy. J. Am. Soc. Nephrol. 19, 34–37 (2008).

    Article  PubMed  Google Scholar 

  113. Rosenstock, J. L. et al. Fibrillary and immunotactoid glomerulonephritis: distinct entities with different clinical and pathologic features. Kidney Int. 63, 1450–1461 (2003).

    Article  PubMed  Google Scholar 

  114. Laurinavicius, A., Hurwitz, S. & Rennke, H. G. Collapsing glomerulopathy in HIV and non-HIV patients: a clinicopathologic and follow-up study. Kidney Int. 56, 2203–2213 (1999).

    Article  CAS  PubMed  Google Scholar 

  115. Austin, H. A. 3rd, Boumpas, D. T., Vaughan, E. M. & Balow, J. E. Predicting renal outcomes in severe lupus nephritis: contributions of clinical and histologic data. Kidney Int. 45, 544–550 (1994).

    Article  PubMed  Google Scholar 

  116. Haas, M. Histologic subclassification of IgA nephropathy: a clinicopathologic study of 244 cases. Am. J. Kidney Dis. 29, 829–842 (1997).

    Article  CAS  PubMed  Google Scholar 

  117. D'Amico, G. Natural history of idiopathic IgA nephropathy: role of clinical and histological prognostic factors. Am. J. Kidney Dis. 36, 227–237 (2000).

    Article  CAS  PubMed  Google Scholar 

Download references

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  1. Division of Renal Diseases and Hypertension, Department of Medicine, George Washington University, 2150 Pennsylvania Avenue, NW #3-438,, Washington, 20037, District of Columbia, USA

    Ehsan Nobakht, Scott D. Cohen & Paul L. Kimmel

  2. Department of Pathology, Johns Hopkins University School of Medicine, 720 Rutland Avenue, Baltimore, 21287, Maryland, USA

    Avi Z. Rosenberg

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  1. Ehsan Nobakht
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  2. Scott D. Cohen
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  3. Avi Z. Rosenberg
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  4. Paul L. Kimmel
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All authors researched the data for the article, provided substantial contributions to discussions of its content, wrote the article, and undertook review and/or editing of the manuscript before submission.

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Correspondence to Scott D. Cohen.

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The authors declare no competing financial interests.

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Nobakht, E., Cohen, S., Rosenberg, A. et al. HIV-associated immune complex kidney disease. Nat Rev Nephrol 12, 291–300 (2016). https://doi.org/10.1038/nrneph.2015.216

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