Нефротоксичность, индуцированная антиангиогенными противоопухолевыми препаратами
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Grechukhina K.S., Chebotareva N.V., Krasnova T.N. Nephrotoxicity of anti-angiogenesis drugs. Therapeutic Archive. 2020; 92 (6): 93–98. DOI: 10.26442/00403660.2020.06.000672
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Ключевые слова: ангиогенез, антиангиогенная терапия, противоопухолевая терапия, нефротический синдром, тромботическая микроангиопатия, нефротоксичность.
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Neoangiogenesis is a basic factor for most physiological as well as pathological processes i.e. tumor metastases. The most important is vascular endothelium growth factor (VEGF) and its’ receptors (VEGFR1/2) in angiogenesis processes. Nowadays antiangiogenic agents (which inhibit VEGF like bevacizumab neither VEGFR2 like ramucirumab) are widely used in very different chemotherapeutic regimens in clinical oncology. The signalling pathway VEGF-VEGFR plays a crucial role in supporting of adequate kidney function. Appearance of antiangiogenic drugs led to adverse nephrotoxic effects: arterial hypertension, proteinuria, rarely – nephrotic syndrome, and kidney dysfunction. Various hystological variants of nephropathy are described, however, in most cases, signs of thrombotic microangiopathy of the renal vessels are noted. This literature review discusses mechanisms, clinical and morphological aspects of nephropathy associated with antiangiogenic drugs.
Keywords: angiogenesis, antiangiogenic therapy, antitumor therapy, nephrotic syndrome, thrombotic microangiopathy, nephrotoxicity.
2. Eremina V, Jefferson J, Kowalewska J. VEGF inhibition and renal thrombotic microangiopathy. N Engl J Med. 2008;358(11):1129-36. doi: 10.1056/NEJMoa0707330
3. Niu G, Chen X. Vascular Endothelial Growth Factor as an Anti-angiogenic Target for Cancer Therapy. Cur Drug Targets. 2010;11(8):1000-17. doi:10.2174/138945010791591395
4. Мещеряков А.А. Антиангиогенная терапия диссеминированного колоректального рака. Современная онкология. 2003;15(3):12-5 [Mesheryakov A. Antiangionenic therapy of disseminated colorectal cancer. Journal of Modern Oncology. 2003;15(3):12-5 (in Russ.)].
5. Трякин А.А. Таргетная терапия колоректального рака, рака желудка и поджелудочной железы. Практическая онкология. 2010;11(3):143-50 [Tryakin A. Target therapy of colorectal, gastric and pancreatic cancers. Practical oncology. 2010;11(3):143-50 (In Russ.)].
6. Giantonio B, Catalano P, Meropol N. Bevacizumab in Combination With Oxaliplatin, Fluorouracil, and Leucovorin (FOLFOX4) for Previously Treated Metastatic Colorectal Cancer: Results From the Eastern Cooperative Oncology Group Study E3200. J Clin Oncol. 2007;20:1539-44. doi: 10.1200/JCO.2006.09.6305
7. Pastorino A, Di Bartolomeo M, Maiello E, et al. Aflibercept Plus
FOLFIRI in the Real-life Setting: Safety and Quality of Life Data From the Italian Patient Cohort of the Aflibercept Safety and Quality-of-Life Program Study. Clin Colorectal Cancer. 2018;17(3):e457-e470. doi: 10.1016/j.clcc.2018.03.002
8. Tabernero J, Takayuki Y, Cohn A. Ramucirumab versus placebo in combination with second- line FOLFIRI in patients with metastatic colorectal carcinoma that progressed during or after first-line therapy with bevacizumab, oxaliplatin, and a fluoropyrimidine (RAISE): a randomised, double-blind, multicentre, phase 3 study. Lancet Oncol. 2015;16:e262. doi: 10.1016/S1470-2045(15)70127
9. Toriu A, et al. Renal-Limited Thrombotic Microangiopathy due to Bevacizumab Therapy for Metastatic Colorectal Cancer: A Case Report. Case Rep Oncol. 2019;12:391-400. doi: 10.1159/00050071
10. Maitland M, Bakris G, Black H, et al. Initial assessment, surveillance, and management of blood pressure in patients receiving vascular endothelial growth factor signaling pathway inhibitors. J Natl Cancer Inst. 2010;102:596-604. doi: 10.1093/jnci/djq091
11. Vaidya V, Ozer J, Frank D, et al. Kidney Injury Molecule-1 Outperforms Traditional Biomarkers of Kidney Injury in Multi-site Preclinical Biomarker Qualification Studies. Nat Biotechnol. 2010;28(5):478-85. doi: 10.1038/nbt.1623
12. Arnold D, Fuchs C, Tabernero J, et al. Meta-analysis of individual patient safety data from six randomized, placebo-controlled trials with the antiangiogenic VEGFR2-binding monoclonal antibody ramucirumab. Ann Oncol. 2017;28:2932-42. doi: 10.1093/annonc/mdx514
13. Qi W, Shen Z, Tang L. Risk of Hypertension in Cancer Patients Treated with Aflibercept: A Systematic Review and Meta-Analysis. Clin Drug Investig. 2014;34:231-40. doi: 10.1007/s40261-014-0174-5
14. Feldman D, Baum M, Ginsberg M, et al. Phase I trial of bevacizumab plus escalated doses ofsunitinib in patients with metastatic renal cell carcinoma. J Clin Oncol. 2009;27:1432-9. doi: 10.1200/JCO.2008.19.0108
15. Azad N, Posadas E, Kwitkowski V, et al. Combination targeted therapy with sorafenib and bevacizumab results in enhanced toxicity and antitumor activity. J Clin Oncol. 2008;26:3709-14. doi: 10.1200/JCO.2007.10.8332
16. Wu S, Chen J, Kudelka A, et al. Incidence and risk of hypertension with sorafenib in patients with cancer: a systematic review and meta-analysis. Lancet Oncol. 2008;9:117-23. doi: 10.1016/j.eururo.2018.05.002
17. Gupta S, Parsa V, Heilbrun L, et al. Safety and efficacy of molecularly targeted agents in patients with metastatic kidney cancer with renal dysfunction. Anticancer Drugs. 2011;22:794-800. doi: 10.1097/CAD.0b013e328346af0d
18. Miura S, Fujino M, Matsuo Y, et al. Nifedipine-induced vascular endothelial growth factor secretion from coronary smooth muscle cells promotes endothelial tube formation via the kinase insert domain-containing receptor/fetal liver kinase-1/NO pathway. Hypertens Res. 2005;28:147-53. doi: 10.1291/hypres.28.147
19. Dirix LY, Maes H, Sweldens C. Treatment of arterial hypertension (AHT) associated with angiogenesis inhibitors. Ann Oncol. 2007;18:1121-2. doi: 10.1093/annonc/mdm205
20. Sugimoto H, Hamano Y, Charytan D, et al. Neutralization of circulating vascular endothelial growth factor (VEGF) by anti-VEGF antibodies and soluble VEGF receptor 1 (sFlt-1) induces proteinuria. J Biol Chem. 2003;278:12605-8. doi:10.1074/jbc.C300012200
21. Eremina V, Sood M, Haigh J, et al. Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. J Clin Invest. 2003;111(5):707-16. doi: 10.1172/JCI17423
22. Zhu X, Wu S, Dahut W, Parikh C. Risks of proteinuria and hypertension with bevacizumab, an antibody against vascular endothelial growth factor: systematic review and meta-analysis. Am J Kidney Dis. 2007;49:186-93. doi: 10.1053/j.ajkd.2006.11.039
23. Yang J, Haworth L, Sherry R, et al. A randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer. N Engl J Med. 2003;349:427-34. doi: 10.1056/NEJMoa021491
24. Patel T, Morgan J, Demetri G, et al. A preeclampsia-like syndrome characterized by reversible hypertension and proteinuria induced by the multitargeted kinase inhibitors sunitinib and sorafenib. J Natl Cancer Inst. 2008;100:282-4. doi: 10.1093/jnci/djm311
25. Miller K, Chap L, Holmes F, et al. Randomized phase III trial of capecitabine compared with bevacizumab plus capecitabine in patients with previously treated metastatic breast cancer. J Clin Oncol. 2005;23:792-9. doi: 10.1200/JCO.2005.05.098
26. Мещеряков А.А. Лечение и профилактика побочных эффектов антиангиогенной терапии у больных метастатическим колоректальным раком. Рос. онкологический журн. 2017;22(3):164-8 [Mesheryakov A. Treatment and prophylaxis of adverse events of antiogenic therapy in patients with colorectal cancer. Russian oncological journal. 2017;22(3):164-8 (In Russ.)]. doi: 10.18821/1028-9984-2017-22-3-164-168
27. Eremina V, Baelde H, Quaggin S. Role of the VEGF – a signaling pathway in the glomerulus: evidence for crosstalk between components of the glomerular filtration barrier. Nephron Physiology. 2007;106(2):32-7. doi: 10.1159/000101798
28. Maynard S, Min J, Merchan J, et al. Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction hypertension, and proteinuria in preeclampsia. J Clin Invest. 2003;111(5):649-58. doi: 10.1172/JCI17189
29. Abrahamson D. Glomerulogenesis in the developing kidney. Semin Nephrol. 1991;4(11):375-89.
30. Eremina V, Sood M, Haigh J, et al. Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. J Clin Invest. 2003;111(5):707-16. doi: 10.1172/JCI17423
31. Hara A, Wada T, Furuchi K, et al. Blockade of VEGF accelerates proteinuria via decrease in nephrin expression in rat crescentic glomerulonephritis. Kidney Int. 2006;69(11):1986-95. doi: 10.1038/sj.ki.5000439
32. Hanna R, et al. Nephrotoxicity induced by intravitreal vascular endothelial growth factor inhibitors: emerging evidence. Kidney Int. 2019;96(3):572-80. doi: 10.1016/j.kint.2019.02.042
33. Diabetic Retinopathy Clinical Research Network, et al. A phase II randomized clinical trial of intravitreal bevacizumab for diabetic macular edema. Ophthalmology. 2007;114(10):1860-7. doi: 10.1016/j.ophtha.2007.05.062
34. Georgalas I, Papaconstantinou D, Papadopoulos K, et al. Renal Injury Following Intravitreal Anti-VEGF Administration in Diabetic Patients with Proliferative Diabetic Retinopathy and Chronic Kidney Disease – A Possible Side Effect? Cur Drug Safety. 2014;9:156. doi: 10.2174/1574886309666140211113635
35. Khneizer P, Gebran T, Al-Taee M, et al. Self-limited membranous nephropathy after intravitreal bevacizumab therapy for age-related macular degeneration. J Nephropathol. 2017;6(3):134-7. doi: 10.15171/jnp.2017.23
36. Morale E, Moliz C, Gutierrez E. Renal damage associated to intravitreal administration of ranibizumab. Nefrología (English Edition). 2017;37(6):653-5. doi: 10.1016/j.nefroe.2017.10.007
37. Eremina V, Quaggin S. Biology of anti-angiogenic therapy-induced thrombotic microangiopathy. Semin Nephrol. 2010;30:582-90. doi: 10.1016/j.semnephrol.2010.09.006
38. Horowitz J, Rivard A, van der Zee R, et al. Vascular endothelial growth factor/vascular permeability factor produces nitric oxide-dependent hypotension. Evidence for a maintenance role in quiescent adult endothelium. Arterioscler Thromb Vasc Biol. 1997;17:2793-800. doi: 10.1161/01.atv.17.11.2793
39. Bollee G, Patey N, Cazajous G, et al. Thrombotic microangiopathy secondary to VEGF pathway inhibition by sunitinib. Nephrol Dial Transplant. 2009;24:682-5. doi: 10.1093/ndt/gfn657
40. Izzedine H, Brocheriou I, Deray G, Rixe O. Thrombotic microangiopathy and anti-VEGF agents. Nephrol Dial Transplant. 2007;22:1481-2. doi: 10.1093/ndt.gfl565
41. Estrada C, Maldonado A, Mallipattu S. Therapeutic Inhibition of VEGF Signaling and Associated Nephrotoxicities. JASN. 2019;30(2):187-200. doi: 10.1681/ASN.2018080853
42. Vicky B, Katarina M, David K. Thrombotic Microangiopathy and the kidney. Clin J Am Soc Nephrol. 2018;13(2):300–17. doi: 10.2215/CJN.00620117
43. Shimamura Y, Maeda T, Takizawa H. Bevacizumab-induced thrombotic microangiopathy and nephrotic syndrome. Clin Exp Nephrol. 2019;23:142-3. doi: 10.1007/s10157-018-1596-9
44. Fujii T, Kawaasoe K, Tonooka A, et al. Nephrotic syndrome associated with ramucirumab therapy. A single-center case series and literature review. Medicine (Baltimore). 2019;98(27):e16236. doi: 10.1097/MD.0000000000016236
45. Izzedine H, Ederhy S, Goldwasser F, et al. Management of hypertension in angiogenesis inhibitor-treated patients. Ann Oncol. 2009;20:807-15. doi: 10.1093/annonc/mdn713
46. Pfister F, Amann K, Daniel C, et al. Characteristic morphological changes in anti-VEGF therapy-induced glomerular microangiopathy. Histopathology. 2018;73(6):990-1001. doi: 10.1111/his.13716
47. Yamada R, Okawa T, Matsuo K, et al. Renal-limited thrombotic microangiopathy after switching from bevacizumab to ramucirumab: a case report. BMC Nephrol. 2019;20(1):14. doi: 10.1186/s12882-018-1194-9
48. Khurana A. Allergic interstitial nephritis possibly related to sunitinib use. Am J Geriatr Pharmacother. 2007;5:341-4. doi: 10.1186/s12882-018-1194-9
49. Nasr S, Snyder R, Bhagat G, Markowitz G. Chronic lymphocytic leukemia and cryoglobulinemic glomerulonephritis. Kidney Int. 2007;71:93. doi: 10.1038/sj.ki.5001891
50. Costero O, Picazo M, Zamora P, et al. Inhibition of tyrosine kinases by sunitinib associated with focal segmental glomerulosclerosis lesion in addition to thrombotic microangiopathy. Nephrol Dial Transplant. 2010;25:1001-3. doi: 10.1093/ndt/gfp666
51. Pellé G, Shweke N, Duong Van Huyen J, et al. Systemic and Kidney Toxicity of Intraocular Administration of Vascular Endothelial Growth Factor Inhibitors. Am J Kidney Dis. 2011;579(5):756-9. doi: 10.1053/j.ajkd.2010.11.030
52. Valdivia M, Mendoza M, Toro Prieto T, et al. Relapse of minimal change disease nephrotic syndrome after administering intravitreal bevacizumab. Nefrología (English Edition). 2014;34(3):373-424. doi: 10.3265/Nefrologia.pre2014.Mar.12388
53. Hanna R, Lopez E, Wilson J, et al. Minimal change disease onset observed after bevacizumab administration. Clin Kidney J. 2016;9(2):239-44. doi: 10.1093/ckj/sfv139
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1. Svetozarskiy N, Artifeksova A, Svetozarskiy S. Vascular endothelial growth factor: biological features and practical significance (literature review). Journal of Siberian Medical Sciences. 2019;4:4-11 (In Russ.)
2. Eremina V, Jefferson J, Kowalewska J. VEGF inhibition and renal thrombotic microangiopathy. N Engl J Med. 2008;358(11):1129-36. doi: 10.1056/NEJMoa0707330
3. Niu G, Chen X. Vascular Endothelial Growth Factor as an Anti-angiogenic Target for Cancer Therapy. Cur Drug Targets. 2010;11(8):1000-17. doi: 10.2174/138945010791591395
4. Mesheryakov A. Antiangionenic therapy of disseminated colorectal cancer. Journal of Modern Oncology. 2003;15(3):12-5 (in Russ.)
5. Tryakin A. Target therapy of colorectal, gastric and pancreatic cancers. Practical oncology. 2010;11(3):143-50 (In Russ.)
6. Giantonio B, Catalano P, Meropol N. Bevacizumab in Combination With Oxaliplatin, Fluorouracil, and Leucovorin (FOLFOX4) for Previously Treated Metastatic Colorectal Cancer: Results From the Eastern Cooperative Oncology Group Study E3200. J Clin Oncol. 2007;20:1539-44. doi: 10.1200/JCO.2006.09.6305
7. Pastorino A, Di Bartolomeo M, Maiello E, et al. Aflibercept Plus
FOLFIRI in the Real-life Setting: Safety and Quality of Life Data From the Italian Patient Cohort of the Aflibercept Safety and Quality-of-Life Program Study. Clin Colorectal Cancer. 2018;17(3):e457-e470. doi: 10.1016/j.clcc.2018.03.002
8. Tabernero J, Takayuki Y, Cohn A. Ramucirumab versus placebo in combination with second- line FOLFIRI in patients with metastatic colorectal carcinoma that progressed during or after first-line therapy with bevacizumab, oxaliplatin, and a fluoropyrimidine (RAISE): a randomised, double-blind, multicentre, phase 3 study. Lancet Oncol. 2015;16:e262. doi: 10.1016/S1470-2045(15)70127
9. Toriu A, et al. Renal-Limited Thrombotic Microangiopathy due to Bevacizumab Therapy for Metastatic Colorectal Cancer: A Case Report. Case Rep Oncol. 2019;12:391-400. doi: 10.1159/00050071
10. Maitland M, Bakris G, Black H, et al. Initial assessment, surveillance, and management of blood pressure in patients receiving vascular endothelial growth factor signaling pathway inhibitors. J Natl Cancer Inst. 2010;102:596-604. doi: 10.1093/jnci/djq091
11. Vaidya V, Ozer J, Frank D, et al. Kidney Injury Molecule-1 Outperforms Traditional Biomarkers of Kidney Injury in Multi-site Preclinical Biomarker Qualification Studies. Nat Biotechnol. 2010;28(5):478-85. doi: 10.1038/nbt.1623
12. Arnold D, Fuchs C, Tabernero J, et al. Meta-analysis of individual patient safety data from six randomized, placebo-controlled trials with the antiangiogenic VEGFR2-binding monoclonal antibody ramucirumab. Ann Oncol. 2017;28:2932-42. doi: 10.1093/annonc/mdx514
13. Qi W, Shen Z, Tang L. Risk of Hypertension in Cancer Patients Treated with Aflibercept: A Systematic Review and Meta-Analysis. Clin Drug Investig. 2014;34:231-40. doi: 10.1007/s40261-014-0174-5
14. Feldman D, Baum M, Ginsberg M, et al. Phase I trial of bevacizumab plus escalated doses ofsunitinib in patients with metastatic renal cell carcinoma. J Clin Oncol. 2009;27:1432-9. doi: 10.1200/JCO.2008.19.0108
15. Azad N, Posadas E, Kwitkowski V, et al. Combination targeted therapy with sorafenib and bevacizumab results in enhanced toxicity and antitumor activity. J Clin Oncol. 2008;26:3709-14. doi: 10.1200/JCO.2007.10.8332
16. Wu S, Chen J, Kudelka A, et al. Incidence and risk of hypertension with sorafenib in patients with cancer: a systematic review and meta-analysis. Lancet Oncol. 2008;9:117-23. doi: 10.1016/j.eururo.2018.05.002
17. Gupta S, Parsa V, Heilbrun L, et al. Safety and efficacy of molecularly targeted agents in patients with metastatic kidney cancer with renal dysfunction. Anticancer Drugs. 2011;22:794-800. doi: 10.1097/CAD.0b013e328346af0d
18. Miura S, Fujino M, Matsuo Y, et al. Nifedipine-induced vascular endothelial growth factor secretion from coronary smooth muscle cells promotes endothelial tube formation via the kinase insert domain-containing receptor/fetal liver kinase-1/NO pathway. Hypertens Res. 2005;28:147-53. doi: 10.1291/hypres.28.147
19. Dirix LY, Maes H, Sweldens C. Treatment of arterial hypertension (AHT) associated with angiogenesis inhibitors. Ann Oncol. 2007;18:1121-2. doi: 10.1093/annonc/mdm205
20. Sugimoto H, Hamano Y, Charytan D, et al. Neutralization of circulating vascular endothelial growth factor (VEGF) by anti-VEGF antibodies and soluble VEGF receptor 1 (sFlt-1) induces proteinuria. J Biol Chem. 2003;278:12605-8. doi: 10.1074/jbc.C300012200
21. Eremina V, Sood M, Haigh J, et al. Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. J Clin Invest. 2003;111(5):707-16. doi: 10.1172/JCI17423
22. Zhu X, Wu S, Dahut W, Parikh C. Risks of proteinuria and hypertension with bevacizumab, an antibody against vascular endothelial growth factor: systematic review and meta-analysis. Am J Kidney Dis. 2007;49:186-93. doi: 10.1053/j.ajkd.2006.11.039
23. Yang J, Haworth L, Sherry R, et al. A randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer. N Engl J Med. 2003;349:427-34. doi: 10.1056/NEJMoa021491
24. Patel T, Morgan J, Demetri G, et al. A preeclampsia-like syndrome characterized by reversible hypertension and proteinuria induced by the multitargeted kinase inhibitors sunitinib and sorafenib. J Natl Cancer Inst. 2008;100:282-4. doi: 10.1093/jnci/djm311
25. Miller K, Chap L, Holmes F, et al. Randomized phase III trial of capecitabine compared with bevacizumab plus capecitabine in patients with previously treated metastatic breast cancer. J Clin Oncol. 2005;23:792-9. doi: 10.1200/JCO.2005.05.098
26. Mesheryakov A. Treatment and prophylaxis of adverse events of antiogenic therapy in patients with colorectal cancer. Russian oncological journal. 2017;22(3):164-8 (In Russ.) doi: 10.18821/1028-9984-2017-22-3-164-168
27. Eremina V, Baelde H, Quaggin S. Role of the VEGF – a signaling pathway in the glomerulus: evidence for crosstalk between components of the glomerular filtration barrier. Nephron Physiology. 2007;106(2):32-7. doi: 10.1159/000101798
28. Maynard S, Min J, Merchan J, et al. Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction hypertension, and proteinuria in preeclampsia. J Clin Invest. 2003;111(5):649-58. doi: 10.1172/JCI17189
29. Abrahamson D. Glomerulogenesis in the developing kidney. Semin Nephrol. 1991;4(11):375-89.
30. Eremina V, Sood M, Haigh J, et al. Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. J Clin Invest. 2003;111(5):707-16. doi: 10.1172/JCI17423
31. Hara A, Wada T, Furuchi K, et al. Blockade of VEGF accelerates proteinuria via decrease in nephrin expression in rat crescentic glomerulonephritis. Kidney Int. 2006;69(11):1986-95. doi: 10.1038/sj.ki.5000439
32. Hanna R, et al. Nephrotoxicity induced by intravitreal vascular endothelial growth factor inhibitors: emerging evidence. Kidney Int. 2019;96(3):572-80. doi: 10.1016/j.kint.2019.02.042
33. Diabetic Retinopathy Clinical Research Network, et al. A phase II randomized clinical trial of intravitreal bevacizumab for diabetic macular edema. Ophthalmology. 2007;114(10):1860-7. doi: 10.1016/j.ophtha.2007.05.062
34. Georgalas I, Papaconstantinou D, Papadopoulos K, et al. Renal Injury Following Intravitreal Anti-VEGF Administration in Diabetic Patients with Proliferative Diabetic Retinopathy and Chronic Kidney Disease – A Possible Side Effect? Cur Drug Safety. 2014;9:156. doi: 10.2174/1574886309666140211113635
35. Khneizer P, Gebran T, Al-Taee M, et al. Self-limited membranous nephropathy after intravitreal bevacizumab therapy for age-related macular degeneration. J Nephropathol. 2017;6(3):134-7. doi: 10.15171/jnp.2017.23
36. Morale E, Moliz C, Gutierrez E. Renal damage associated to intravitreal administration of ranibizumab. Nefrología (English Edition). 2017;37(6):653-5. doi: 10.1016/j.nefroe.2017.10.007
37. Eremina V, Quaggin S. Biology of anti-angiogenic therapy-induced thrombotic microangiopathy. Semin Nephrol. 2010;30:582-90. doi: 10.1016/j.semnephrol.2010.09.006
38. Horowitz J, Rivard A, van der Zee R, et al. Vascular endothelial growth factor/vascular permeability factor produces nitric oxide-dependent hypotension. Evidence for a maintenance role in quiescent adult endothelium. Arterioscler Thromb Vasc Biol. 1997;17:2793-800. doi: 10.1161/01.atv.17.11.2793
39. Bollee G, Patey N, Cazajous G, et al. Thrombotic microangiopathy secondary to VEGF pathway inhibition by sunitinib. Nephrol Dial Transplant. 2009;24:682-5. doi: 10.1093/ndt/gfn657
40. Izzedine H, Brocheriou I, Deray G, Rixe O. Thrombotic microangiopathy and anti-VEGF agents. Nephrol Dial Transplant. 2007;22:1481-2. doi: 10.1093/ndt.gfl565
41. Estrada C, Maldonado A, Mallipattu S. Therapeutic Inhibition of VEGF Signaling and Associated Nephrotoxicities. JASN. 2019;30(2):187-200. doi: 10.1681/ASN.2018080853
42. Vicky B, Katarina M, David K. Thrombotic Microangiopathy and the kidney. Clin J Am Soc Nephrol. 2018;13(2):300–17. doi: 10.2215/CJN.00620117
43. Shimamura Y, Maeda T, Takizawa H. Bevacizumab-induced thrombotic microangiopathy and nephrotic syndrome. Clin Exp Nephrol. 2019;23:142-3. doi: 10.1007/s10157-018-1596-9
44. Fujii T, Kawaasoe K, Tonooka A, et al. Nephrotic syndrome associated with ramucirumab therapy. A single-center case series and literature review. Medicine (Baltimore). 2019;98(27):e16236. doi: 10.1097/MD.0000000000016236
45. Izzedine H, Ederhy S, Goldwasser F, et al. Management of hypertension in angiogenesis inhibitor-treated patients. Ann Oncol. 2009;20:807-15. doi: 10.1093/annonc/mdn713
46. Pfister F, Amann K, Daniel C, et al. Characteristic morphological changes in anti-VEGF therapy-induced glomerular microangiopathy. Histopathology. 2018;73(6):990-1001. doi: 10.1111/his.13716
47. Yamada R, Okawa T, Matsuo K, et al. Renal-limited thrombotic microangiopathy after switching from bevacizumab to ramucirumab: a case report. BMC Nephrol. 2019;20(1):14. doi: 10.1186/s12882-018-1194-9
48. Khurana A. Allergic interstitial nephritis possibly related to sunitinib use. Am J Geriatr Pharmacother. 2007;5:341-4. doi: 10.1186/s12882-018-1194-9
49. Nasr S, Snyder R, Bhagat G, Markowitz G. Chronic lymphocytic leukemia and cryoglobulinemic glomerulonephritis. Kidney Int. 2007;71:93. doi: 10.1038/sj.ki.5001891
50. Costero O, Picazo M, Zamora P, et al. Inhibition of tyrosine kinases by sunitinib associated with focal segmental glomerulosclerosis lesion in addition to thrombotic microangiopathy. Nephrol Dial Transplant. 2010;25:1001-3. doi: 10.1093/ndt/gfp666
51. Pellé G, Shweke N, Duong Van Huyen J, et al. Systemic and Kidney Toxicity of Intraocular Administration of Vascular Endothelial Growth Factor Inhibitors. Am J Kidney Dis. 2011;579(5):756-9. doi: 10.1053/j.ajkd.2010.11.030
52. Valdivia M, Mendoza M, Toro Prieto T, et al. Relapse of minimal change disease nephrotic syndrome after administering intravitreal bevacizumab. Nefrología (English Edition). 2014;34(3):373-424. doi: 10.3265/Nefrologia.pre2014.Mar.12388
53. Hanna R, Lopez E, Wilson J, et al. Minimal change disease onset observed after bevacizumab administration. Clin Kidney J. 2016;9(2):239-44. doi: 10.1093/ckj/sfv139
1 ФГБОУ ВО «Московский государственный университет им. М.В. Ломоносова», Москва, Россия;
2 ГБУЗ «Московский клинический научно-практический центр им. А.С. Логинова» Департамента здравоохранения г. Москвы,
Москва, Россия;
3 ФГАОУ ВО «Первый Московский государственный медицинский университет им. И.М. Сеченова» Минздрава России
(Сеченовский Университет), Москва, Россия
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K.S. Grechukhina1,2, N.V. Chebotareva3, T.N. Krasnova1
1 Lomonosov Moscow State University, Moscow, Russia;
2 Loginov Moscow Clinical Scientific Center, Moscow, Russia;
3 Sechenov First Moscow State Medical University (Sechenov University), Moscow, Russia