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THE IMPORTANCE OF GLOMERULAR C3 ACCUMULATION IN ELDERLY PATIENTS WITH PRIMARY MEMBRANOUS NEPHROPATHY

Year 2022, Volume: 85 Issue: 4, 541 - 547, 28.10.2022
https://doi.org/10.26650/IUITFD.1126241

Abstract

ABSTRACT Objective: The purpose of this study was to investigate the impact of glomerular C3 accumulation density on clinical, histopathological parameters and outcomes in elderly (>60 years) individuals with primary membranous nephropathy (PMN). Material and Methods: In this study, we examined the patients (n=105) in two groups according to the C3 staining density in kidney biopsy samples as low intensity (C3: 1+; LI group) and high intensity (C3: 2+ or C3: 3+; HI group). The primary endpoint of our study was the end-stage renal disease, and the secondary endpoints were the development of partial remission (PR) or complete remission (CR). Results: At the end of the follow-up (mean 30.6 months), more patients achieved the primary endpoint, and fewer patients achieved the secondary endpoints in the HI group compared to the LI group. (p=0.015 and p=0.016, respectively). Moreover, the glomerular filtration rate (eGFR) was lower (p<0.001), and proteinuria was higher in the HI group (p=0.018). Kaplan-Meier survival analysis revealed that renal survival (p=0.031) was lower in the HI group compared to the LI group. In the multivariate logistic regression analyses, no predictive parameters could be detected for the endpoints. Conclusion: Intense glomerular C3 deposition in elderly (>60 years) patients with PMN may be related to poor clinical outcomes. 

Supporting Institution

NA

Project Number

NA

References

  • 1. Glassock RJ. The pathogenesis of idiopathic membranous nephropathy: A 50-year odyssey. Am J Kidney Dis 2010;56(1):157-67. [CrossRef] google scholar
  • 2. Zeng CH, Chen HM, Wang RS, Chen Y, Zhang SH, Liu L, et al. Etiology and clinical characteristics of membranous nephropathy in Chinese patients. Am J Kidney Dis 2008;52(4):691-8. [CrossRef] google scholar
  • 3. Feng Z, Wang S, Huang Y, Liang X, Shi W, Zhang B. A follow-up analysis of positron emission tomography/computed tomography in detecting hidden malignancies at the time of diagnosis of membranous nephropathy. Oncotarget 2016;7(9):9645. [CrossRef] google scholar
  • 4. Seitz-Polski B, Dolla G, Payre C, Girard CA, Polidori J, Zorzi K, et al. Epitope spreading of autoantibody response to PLA2R associates with poor prognosis in membranous nephropathy. J Am Soc Nephrol 2016;27(5):1517-33. [CrossRef] google scholar
  • 5. Beck Jr LH, Bonegio RG, Lambeau G, Beck DM, Powell DW, Cummins TD, et al. M-type phospholipase A2 receptor as target antigen in idiopathic membranous nephropathy. N Engl J Med 2009;361(1):11-21. [CrossRef] google scholar
  • 6. Tomas NM, Beck Jr LH, Meyer-Schwesinger C, Seitz-Polski B, Ma H, Zahner G, et al. Thrombospondin type-1 domain-containing 7A in idiopathic membranous nephropathy. N Engl J Med 2014;371(24):2277-87. [CrossRef] google scholar
  • 7. Sethi S, Madden BJ, Debiec H, Charlesworth MC, Gross L, Ravindran A, et al. Exostosin 1/exostosin 2-associated membranous nephropathy. J Am Soc Nephrol 2019;30(6):1123-36. [CrossRef] google scholar
  • 8. Pei Y, Cattran D, Greenwood C. Predicting chronic renal insufficiency in idiopathic membranous glomerulonephritis. Kidney Int 1992;42(4):960-6. [CrossRef] google scholar
  • 9. Schieppati A, Mosconi L, Perna A, Mecca G, Bertani T, Garattini S, et al. prognosis of untreated patients with idiopathic membranous nephropathy. N Engl J Med 1993;329(2):85-9. [CrossRef] google scholar
  • 10. Kanigicherla D, Gummadova J, McKenzie EA, Roberts SA, Harris S, Nikam M, et al. Anti-PLA2R antibodies measured by ELISA predict long-term outcome in a prevalent population of patients with idiopathic membranous nephropathy. Kidney Int 2013;83(5):940-8. [CrossRef] google scholar
  • 11. Davison A, Cameron J, Kerr D, Ogg C, Wilkinson R. The natural history of renal function in untreated idiopathic membranous glomerulonephritis in adults. Clin Nephrol 1984;22(2):61-7. google scholar
  • 12. Ma H, Sandor DG, Beck Jr LH. The role of complement in membranous nephropathy. Semin Nephrol 2013;33(6):531-42. [CrossRef] google scholar
  • 13. Sethi S, Nasr SH, De Vriese AS, Fervenza FC. C4d as a diagnostic tool in proliferative GN. J Am Soc Nephrol 2015;26(11):2852-9. [CrossRef] google scholar
  • 14. Ma H, Sandor DG, Beck LH, Jr. The role of complement in membranous nephropathy. Semin Nephrol 2013;33(6):531-42. [CrossRef] google scholar
  • 15. Oto OA, Demir E, Mirioglu S, Dirim AB, Ozluk Y, Cebeci E, et al. Clinical significance of glomerular C3 deposition in primary membranous nephropathy. J Nephrol 2021;34(2):581-7. [CrossRef] google scholar
  • 16. Ricklin D, Reis ES, Lambris JD. Complement in disease: a defence system turning offensive. Nat Rev Nephrol 2016;12(7):383-401. [CrossRef] google scholar
  • 17. Liu H, Fergusson MM, Castilho RM, Liu J, Cao L, Chen J, et al. Augmented Wnt signaling in a mammalian model of accelerated aging. Science 2007;317(5839):803-06. [CrossRef] google scholar 18. Liu D, Lun L, Huang Q, Ning Y, Zhang Y, Wang L, et al. Youthful systemic milieu alleviates renal ischemia-reperfusion injury in elderly mice. Kidney Int 2018;94(2):268-79. [CrossRef] google scholar
  • 19. Cattran DC, Appel GB, Hebert LA, Hunsicker LG, Pohl MA, Hoy WE, et al. Cyclosporine in patients with steroid-resistant membranous nephropathy: A randomized trial. Kidney Int 2001;59(4):1484-90. [CrossRef] google scholar
  • 20. Cattran DC, Feehally J, Cook HT, Liu ZH, Fervenza F, Mezzano S, et al. Kidney disease: Improving global outcomes (KDIGO) glomerulonephritis work group. KDIGO clinical practice guideline for glomerulonephritis. Kidney Int Supplements 2012;2:139-274. google scholar
  • 21. Ehrenreich T, Porush JG, Churg J, Garfinkel L, Glabman S, Goldstein MH, et al. Treatment of idiopathic membranous nephropathy. N Engl J Med 1976;295(14):741-6. [CrossRef] google scholar
  • 22. Franzin R, Stasi A, Fiorentino M, Stallone G, Cantaluppi V, Gesualdo L, et al. Inflammaging and Complement System: A Link Between Acute Kidney Injury and Chronic Graft Damage. Front Immunol 2020;11:734. [CrossRef] google scholar
  • 23. McGeer EG, Klegeris A, McGeer PL. Inflammation, the complement system and the diseases of aging. Neurobiol Aging 2005;26(1):94-7. [CrossRef] google scholar
  • 24. Cribbs DH, Berchtold NC, Perreau V, Coleman PD, Rogers J, Tenner AJ, et al. Extensive innate immune gene activation accompanies brain aging, increasing vulnerability to cognitive decline and neurodegeneration: a microarray study. J Neuroinflammation 2012;9(1):1-18. [CrossRef] google scholar
  • 25. Stephan AH, Madison DV, Mateos JM, Fraser DA, Lovelett EA, Coutellier L, et al. A dramatic increase of C1q protein in the CNS during normal aging. J Neurosci 2013;33(33):13460-74. [CrossRef] google scholar 26. Ricklin D, Reis ES, Lambris JD. Complement in disease: a defence system turning offensive. Nat Rev Nephrol 2016;12(7):383-401. [CrossRef] google scholar
  • 27. Castellano G, Trouw LA, Fiore N, Daha MR, Schena FP, van Kooten C. Infiltrating dendritic cells contribute to local synthesis of C1q in murine and human lupus nephritis. Mol Immunol 2010;47(11-12):2129-37. [CrossRef] google scholar
  • 28. Fearn A, Sheerin NS. Complement activation in progressive renal disease. World J Nephrol 2015;4(1):31-40. [CrossRef] google scholar
  • 29. Thurman JM. Complement in kidney disease: core curriculum 2015. Am J Kidney Dis 2015;65(1):156-68. [CrossRef] google scholar
  • 30. Erwin D. The clinical course of idiopathic membranous nephropathy. Mayo Clin Proc 1973;48:697-712. google scholar
  • 31. Beregi E, Varga I. Analysis of 260 cases of membranous glomerulonephritis in renal biopsy material. Clin Nephrol 1974;2(6):215-21. google scholar
  • 32. Abe S, Amagasaki Y, Konishi K, Kato E, Iyori S, Sakaguchi H. Idiopathic membranous glomerulonephritis: aspects of geographical differences. J Clin Pathol 1986;39(11):1193-8. [CrossRef] google scholar
  • 33. Brenchley PE, Coupes B, Short CD, O’Donoghue DJ, Ballardie FW, Mallick NP. Urinary C3dg and C5b-9 indicate active immune disease in human membranous nephropathy. Kidney Int 1992;41(4):933-7. [CrossRef] google scholar
  • 34. Segawa Y, Hisano S, Matsushita M, Fujita T, Hirose S, Takeshita M, et al. IgG subclasses and complement pathway in segmental and global membranous nephropathy. Ped Nephrol 2010;25(6):1091-9. [CrossRef] google scholar
  • 35. Borza DB. Alternative pathway dysregulation and the conundrum of complement activation by IgG4 immune complexes in membranous nephropathy. Front Immunol 2016;7:157. [CrossRef] google scholar
  • 36. Marx BE, Marx M. Prediction in idiopathic membranous nephropathy. Kidney Int 1999;56(2):666-73. [CrossRef] google scholar
  • 37. Troyanov S, Roasio L, Pandes M, Herzenberg A, Cattran D. Renal pathology in idiopathic membranous nephropathy: a new perspective. Kidney Int 2006;69(9):1641-8. [CrossRef] google scholar
  • 38. Zhang XD, Cui Z, Zhang MF, Wang J, Zhang YM, Qu Z, et al. Clinical implications of pathological features of primary membranous nephropathy. BMC Nephrol 2018;19(1):1-9. [CrossRef] google scholar
  • 39. Yoshimoto K, Yokoyama H, Wada T, Furuichi K, Sakai N, Iwata Y, et al. Pathologic findings of initial biopsies reflect the outcomes of membranous nephropathy. Kidney Int 2004;65(1):148-53. [CrossRef] google scholar
  • 40. Cattran D. Management of membranous nephropathy: when and what for treatment. J Am Soc Nephrol 2005;16(5):1188-94. [CrossRef] google scholar
  • 41. Sprangers B, Bomback AS, Cohen SD, Radhakrishnan J, Valeri A, Markowitz GS, et al. Idiopathic membranous nephropathy: clinical and histologic prognostic features and treatment patterns over time at a tertiary referral center. Am J Nephrol 2012;36(1):78-89. [CrossRef] google scholar

İLERİ YAŞLI PRİMER MEMBRANÖZ NEFROPATİLİ HASTALARDA GLOMERÜLER C3 BİRİKİMİNİN ÖNEMİ

Year 2022, Volume: 85 Issue: 4, 541 - 547, 28.10.2022
https://doi.org/10.26650/IUITFD.1126241

Abstract

Amaç: Bu çalışmada, primer membranöz nefropatili (PMN) yaşlı (>60 yaş) hastalarda glomerüler C3 birikim yoğunluğunun klinik, histopatolojik özellikler ve hastalığın seyri üzerindeki etkilerini araştırmayı amaçladık. Gereç ve Yöntem: Bu retrospektif gözlemsel çalışmaya dahil ettiğimiz PMN’li 105 hastayı böbrek biyopsi örneklerinde C3 birikiminin yoğunluğuna göre düşük yoğunluklu (C3 1+; LI) ve yüksek yoğunluklu (C3 2+ veya C3 3+; HI) olmak üzere iki grupta inceledik. Birincil sonlanım noktası son evre böbrek hastalığı, ikincil sonlanım noktaları ise tam (CR) veya kısmi remisyon (PR) idi. Bulgular: İzlem sonunda (ortanca 30,6 ay), HI grubunda LI grubuna kıyasla daha fazla hasta birincil noktaya ulaşırken daha az hasta ikincil son noktalara erişti (sırasıyla p=0,015 ve p=0,016). Ayrıca HI grubunda LI grubuna göre glomerüler filtrasyon hızı (eGFR) daha düşük (p<0,001), proteinüri ise daha fazlaydı (p=0,018). Kaplan-Meier analizlerinde böbrek sağ kalımının (p=0,031) HI grubunda LI grubundan daha düşük olduğu saptandı. Çok değişkenli lojistik regresyon analizlerinde, son noktalar öngördürücü bir parametre saptanamadı. Sonuç: Yoğun glomerüler C3 birikimi, PMN’li yaşlı hastalarda olumsuz klinik sonuçlarla ilişkilidir. 

Project Number

NA

References

  • 1. Glassock RJ. The pathogenesis of idiopathic membranous nephropathy: A 50-year odyssey. Am J Kidney Dis 2010;56(1):157-67. [CrossRef] google scholar
  • 2. Zeng CH, Chen HM, Wang RS, Chen Y, Zhang SH, Liu L, et al. Etiology and clinical characteristics of membranous nephropathy in Chinese patients. Am J Kidney Dis 2008;52(4):691-8. [CrossRef] google scholar
  • 3. Feng Z, Wang S, Huang Y, Liang X, Shi W, Zhang B. A follow-up analysis of positron emission tomography/computed tomography in detecting hidden malignancies at the time of diagnosis of membranous nephropathy. Oncotarget 2016;7(9):9645. [CrossRef] google scholar
  • 4. Seitz-Polski B, Dolla G, Payre C, Girard CA, Polidori J, Zorzi K, et al. Epitope spreading of autoantibody response to PLA2R associates with poor prognosis in membranous nephropathy. J Am Soc Nephrol 2016;27(5):1517-33. [CrossRef] google scholar
  • 5. Beck Jr LH, Bonegio RG, Lambeau G, Beck DM, Powell DW, Cummins TD, et al. M-type phospholipase A2 receptor as target antigen in idiopathic membranous nephropathy. N Engl J Med 2009;361(1):11-21. [CrossRef] google scholar
  • 6. Tomas NM, Beck Jr LH, Meyer-Schwesinger C, Seitz-Polski B, Ma H, Zahner G, et al. Thrombospondin type-1 domain-containing 7A in idiopathic membranous nephropathy. N Engl J Med 2014;371(24):2277-87. [CrossRef] google scholar
  • 7. Sethi S, Madden BJ, Debiec H, Charlesworth MC, Gross L, Ravindran A, et al. Exostosin 1/exostosin 2-associated membranous nephropathy. J Am Soc Nephrol 2019;30(6):1123-36. [CrossRef] google scholar
  • 8. Pei Y, Cattran D, Greenwood C. Predicting chronic renal insufficiency in idiopathic membranous glomerulonephritis. Kidney Int 1992;42(4):960-6. [CrossRef] google scholar
  • 9. Schieppati A, Mosconi L, Perna A, Mecca G, Bertani T, Garattini S, et al. prognosis of untreated patients with idiopathic membranous nephropathy. N Engl J Med 1993;329(2):85-9. [CrossRef] google scholar
  • 10. Kanigicherla D, Gummadova J, McKenzie EA, Roberts SA, Harris S, Nikam M, et al. Anti-PLA2R antibodies measured by ELISA predict long-term outcome in a prevalent population of patients with idiopathic membranous nephropathy. Kidney Int 2013;83(5):940-8. [CrossRef] google scholar
  • 11. Davison A, Cameron J, Kerr D, Ogg C, Wilkinson R. The natural history of renal function in untreated idiopathic membranous glomerulonephritis in adults. Clin Nephrol 1984;22(2):61-7. google scholar
  • 12. Ma H, Sandor DG, Beck Jr LH. The role of complement in membranous nephropathy. Semin Nephrol 2013;33(6):531-42. [CrossRef] google scholar
  • 13. Sethi S, Nasr SH, De Vriese AS, Fervenza FC. C4d as a diagnostic tool in proliferative GN. J Am Soc Nephrol 2015;26(11):2852-9. [CrossRef] google scholar
  • 14. Ma H, Sandor DG, Beck LH, Jr. The role of complement in membranous nephropathy. Semin Nephrol 2013;33(6):531-42. [CrossRef] google scholar
  • 15. Oto OA, Demir E, Mirioglu S, Dirim AB, Ozluk Y, Cebeci E, et al. Clinical significance of glomerular C3 deposition in primary membranous nephropathy. J Nephrol 2021;34(2):581-7. [CrossRef] google scholar
  • 16. Ricklin D, Reis ES, Lambris JD. Complement in disease: a defence system turning offensive. Nat Rev Nephrol 2016;12(7):383-401. [CrossRef] google scholar
  • 17. Liu H, Fergusson MM, Castilho RM, Liu J, Cao L, Chen J, et al. Augmented Wnt signaling in a mammalian model of accelerated aging. Science 2007;317(5839):803-06. [CrossRef] google scholar 18. Liu D, Lun L, Huang Q, Ning Y, Zhang Y, Wang L, et al. Youthful systemic milieu alleviates renal ischemia-reperfusion injury in elderly mice. Kidney Int 2018;94(2):268-79. [CrossRef] google scholar
  • 19. Cattran DC, Appel GB, Hebert LA, Hunsicker LG, Pohl MA, Hoy WE, et al. Cyclosporine in patients with steroid-resistant membranous nephropathy: A randomized trial. Kidney Int 2001;59(4):1484-90. [CrossRef] google scholar
  • 20. Cattran DC, Feehally J, Cook HT, Liu ZH, Fervenza F, Mezzano S, et al. Kidney disease: Improving global outcomes (KDIGO) glomerulonephritis work group. KDIGO clinical practice guideline for glomerulonephritis. Kidney Int Supplements 2012;2:139-274. google scholar
  • 21. Ehrenreich T, Porush JG, Churg J, Garfinkel L, Glabman S, Goldstein MH, et al. Treatment of idiopathic membranous nephropathy. N Engl J Med 1976;295(14):741-6. [CrossRef] google scholar
  • 22. Franzin R, Stasi A, Fiorentino M, Stallone G, Cantaluppi V, Gesualdo L, et al. Inflammaging and Complement System: A Link Between Acute Kidney Injury and Chronic Graft Damage. Front Immunol 2020;11:734. [CrossRef] google scholar
  • 23. McGeer EG, Klegeris A, McGeer PL. Inflammation, the complement system and the diseases of aging. Neurobiol Aging 2005;26(1):94-7. [CrossRef] google scholar
  • 24. Cribbs DH, Berchtold NC, Perreau V, Coleman PD, Rogers J, Tenner AJ, et al. Extensive innate immune gene activation accompanies brain aging, increasing vulnerability to cognitive decline and neurodegeneration: a microarray study. J Neuroinflammation 2012;9(1):1-18. [CrossRef] google scholar
  • 25. Stephan AH, Madison DV, Mateos JM, Fraser DA, Lovelett EA, Coutellier L, et al. A dramatic increase of C1q protein in the CNS during normal aging. J Neurosci 2013;33(33):13460-74. [CrossRef] google scholar 26. Ricklin D, Reis ES, Lambris JD. Complement in disease: a defence system turning offensive. Nat Rev Nephrol 2016;12(7):383-401. [CrossRef] google scholar
  • 27. Castellano G, Trouw LA, Fiore N, Daha MR, Schena FP, van Kooten C. Infiltrating dendritic cells contribute to local synthesis of C1q in murine and human lupus nephritis. Mol Immunol 2010;47(11-12):2129-37. [CrossRef] google scholar
  • 28. Fearn A, Sheerin NS. Complement activation in progressive renal disease. World J Nephrol 2015;4(1):31-40. [CrossRef] google scholar
  • 29. Thurman JM. Complement in kidney disease: core curriculum 2015. Am J Kidney Dis 2015;65(1):156-68. [CrossRef] google scholar
  • 30. Erwin D. The clinical course of idiopathic membranous nephropathy. Mayo Clin Proc 1973;48:697-712. google scholar
  • 31. Beregi E, Varga I. Analysis of 260 cases of membranous glomerulonephritis in renal biopsy material. Clin Nephrol 1974;2(6):215-21. google scholar
  • 32. Abe S, Amagasaki Y, Konishi K, Kato E, Iyori S, Sakaguchi H. Idiopathic membranous glomerulonephritis: aspects of geographical differences. J Clin Pathol 1986;39(11):1193-8. [CrossRef] google scholar
  • 33. Brenchley PE, Coupes B, Short CD, O’Donoghue DJ, Ballardie FW, Mallick NP. Urinary C3dg and C5b-9 indicate active immune disease in human membranous nephropathy. Kidney Int 1992;41(4):933-7. [CrossRef] google scholar
  • 34. Segawa Y, Hisano S, Matsushita M, Fujita T, Hirose S, Takeshita M, et al. IgG subclasses and complement pathway in segmental and global membranous nephropathy. Ped Nephrol 2010;25(6):1091-9. [CrossRef] google scholar
  • 35. Borza DB. Alternative pathway dysregulation and the conundrum of complement activation by IgG4 immune complexes in membranous nephropathy. Front Immunol 2016;7:157. [CrossRef] google scholar
  • 36. Marx BE, Marx M. Prediction in idiopathic membranous nephropathy. Kidney Int 1999;56(2):666-73. [CrossRef] google scholar
  • 37. Troyanov S, Roasio L, Pandes M, Herzenberg A, Cattran D. Renal pathology in idiopathic membranous nephropathy: a new perspective. Kidney Int 2006;69(9):1641-8. [CrossRef] google scholar
  • 38. Zhang XD, Cui Z, Zhang MF, Wang J, Zhang YM, Qu Z, et al. Clinical implications of pathological features of primary membranous nephropathy. BMC Nephrol 2018;19(1):1-9. [CrossRef] google scholar
  • 39. Yoshimoto K, Yokoyama H, Wada T, Furuichi K, Sakai N, Iwata Y, et al. Pathologic findings of initial biopsies reflect the outcomes of membranous nephropathy. Kidney Int 2004;65(1):148-53. [CrossRef] google scholar
  • 40. Cattran D. Management of membranous nephropathy: when and what for treatment. J Am Soc Nephrol 2005;16(5):1188-94. [CrossRef] google scholar
  • 41. Sprangers B, Bomback AS, Cohen SD, Radhakrishnan J, Valeri A, Markowitz GS, et al. Idiopathic membranous nephropathy: clinical and histologic prognostic features and treatment patterns over time at a tertiary referral center. Am J Nephrol 2012;36(1):78-89. [CrossRef] google scholar
There are 39 citations in total.

Details

Primary Language English
Subjects Health Care Administration
Journal Section RESEARCH
Authors

Özgür Akın Oto 0000-0003-0928-8103

Safak Mırıoglu 0000-0003-0362-8154

Ahmet Burak Dirim 0000-0003-2262-8627

Seda Şafak 0000-0002-5431-7754

Nurana Güller This is me 0000-0002-3170-7346

Erol Demir 0000-0003-0128-5645

Ayşe Serra Artan 0000-0002-6461-3178

Yasemin Özlük 0000-0002-7191-0488

Ali Rıza Uçar 0000-0003-1812-1911

Lala Soltanova 0000-0002-4420-4721

Kanan Nuriyev 0000-0003-3806-6200

Halil Yazıcı 0000-0003-2526-3483

Yasar Calıskan 0000-0003-2526-3483

Project Number NA
Publication Date October 28, 2022
Submission Date June 5, 2022
Published in Issue Year 2022 Volume: 85 Issue: 4

Cite

APA Oto, Ö. A., Mırıoglu, S., Dirim, A. B., Şafak, S., et al. (2022). THE IMPORTANCE OF GLOMERULAR C3 ACCUMULATION IN ELDERLY PATIENTS WITH PRIMARY MEMBRANOUS NEPHROPATHY. Journal of Istanbul Faculty of Medicine, 85(4), 541-547. https://doi.org/10.26650/IUITFD.1126241
AMA Oto ÖA, Mırıoglu S, Dirim AB, Şafak S, Güller N, Demir E, Artan AS, Özlük Y, Uçar AR, Soltanova L, Nuriyev K, Yazıcı H, Calıskan Y. THE IMPORTANCE OF GLOMERULAR C3 ACCUMULATION IN ELDERLY PATIENTS WITH PRIMARY MEMBRANOUS NEPHROPATHY. İst Tıp Fak Derg. October 2022;85(4):541-547. doi:10.26650/IUITFD.1126241
Chicago Oto, Özgür Akın, Safak Mırıoglu, Ahmet Burak Dirim, Seda Şafak, Nurana Güller, Erol Demir, Ayşe Serra Artan, Yasemin Özlük, Ali Rıza Uçar, Lala Soltanova, Kanan Nuriyev, Halil Yazıcı, and Yasar Calıskan. “THE IMPORTANCE OF GLOMERULAR C3 ACCUMULATION IN ELDERLY PATIENTS WITH PRIMARY MEMBRANOUS NEPHROPATHY”. Journal of Istanbul Faculty of Medicine 85, no. 4 (October 2022): 541-47. https://doi.org/10.26650/IUITFD.1126241.
EndNote Oto ÖA, Mırıoglu S, Dirim AB, Şafak S, Güller N, Demir E, Artan AS, Özlük Y, Uçar AR, Soltanova L, Nuriyev K, Yazıcı H, Calıskan Y (October 1, 2022) THE IMPORTANCE OF GLOMERULAR C3 ACCUMULATION IN ELDERLY PATIENTS WITH PRIMARY MEMBRANOUS NEPHROPATHY. Journal of Istanbul Faculty of Medicine 85 4 541–547.
IEEE Ö. A. Oto, “THE IMPORTANCE OF GLOMERULAR C3 ACCUMULATION IN ELDERLY PATIENTS WITH PRIMARY MEMBRANOUS NEPHROPATHY”, İst Tıp Fak Derg, vol. 85, no. 4, pp. 541–547, 2022, doi: 10.26650/IUITFD.1126241.
ISNAD Oto, Özgür Akın et al. “THE IMPORTANCE OF GLOMERULAR C3 ACCUMULATION IN ELDERLY PATIENTS WITH PRIMARY MEMBRANOUS NEPHROPATHY”. Journal of Istanbul Faculty of Medicine 85/4 (October 2022), 541-547. https://doi.org/10.26650/IUITFD.1126241.
JAMA Oto ÖA, Mırıoglu S, Dirim AB, Şafak S, Güller N, Demir E, Artan AS, Özlük Y, Uçar AR, Soltanova L, Nuriyev K, Yazıcı H, Calıskan Y. THE IMPORTANCE OF GLOMERULAR C3 ACCUMULATION IN ELDERLY PATIENTS WITH PRIMARY MEMBRANOUS NEPHROPATHY. İst Tıp Fak Derg. 2022;85:541–547.
MLA Oto, Özgür Akın et al. “THE IMPORTANCE OF GLOMERULAR C3 ACCUMULATION IN ELDERLY PATIENTS WITH PRIMARY MEMBRANOUS NEPHROPATHY”. Journal of Istanbul Faculty of Medicine, vol. 85, no. 4, 2022, pp. 541-7, doi:10.26650/IUITFD.1126241.
Vancouver Oto ÖA, Mırıoglu S, Dirim AB, Şafak S, Güller N, Demir E, Artan AS, Özlük Y, Uçar AR, Soltanova L, Nuriyev K, Yazıcı H, Calıskan Y. THE IMPORTANCE OF GLOMERULAR C3 ACCUMULATION IN ELDERLY PATIENTS WITH PRIMARY MEMBRANOUS NEPHROPATHY. İst Tıp Fak Derg. 2022;85(4):541-7.

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