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Saudi Journal of Kidney Diseases and Transplantation
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Year : 2020  |  Volume : 31  |  Issue : 1  |  Page : 182-190
Predictors of renal outcomes in anti-neutrophil cytoplasmic antibody glomerulonephritis


1 Department of Nephrology, Dialysis and Transplantation, La Rabta Hospital, Tunis, Tunisia
2 Department of Immunology, Dialysis and Transplantation, La Rabta Hospital, Tunis, Tunisia
3 Research Laboratory of Kidney Diseases (LR00SP01), Charles Nicolle Hospital, Tunis, Tunisia
4 Department of Nephrology, Kef Hospital, Kef, Tunisia
5 Department of Internal Medicine, La Rabta Hospital, Tunis, Tunisia

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Date of Submission04-Mar-2019
Date of Acceptance29-Apr-2019
Date of Web Publication3-Mar-2020
 

   Abstract 


Glomerulonephritis associated with anti-neutrophil cytoplasmic antibody (ANCA) vasculitis still has a high prevalence of end-stage renal disease (ESRD), particularly in patients with advanced renal failure at presentation. This study aims to evaluate the clinical and histo- pathological features of renal involvement and investigate factors associated with ESRD. Patients with renal biopsy-proven ANCA-associated glomerulonephritis were included retrospectively over a period of nine years (June 2007 to March 2016). The renal survival, defined as time to reach ESRD, was evaluated based on clinical parameters, histopathological classification, and renal risk score. A total of 37 patients with crescentic glomerulonephritis were included in the study. The average age was 54 ± 16 years (range: 17-80) and 51.3% were female. Twenty-two patients were diagnosed with microscopic polyangiitis and 15 had granulomatosis with polyangiitis. The median glomerular filtration rate at presentation was 16.73 mL/min/1.73 m2. Thirty-five patients (94.5%) had renal failure at presentation and 23 patients (62.1%) required initial hemodialysis (HD) therapy. The pattern of glomerular injury was categorized as sclerotic in 48.6% of cases, crescentic in 24.3%, mixed in 24.3%, and focal class in 2.7%. Regarding renal risk score, we had five patients with low risk, 17 with intermediate risk and 15 with high risk. ESRD occurred in 47% of intermediate-risk group and 66% of the high risk group. During follow-up, 17 patients (45.9%) developed ESRD. Tobacco addiction (P = 0.02), alveolar hemorrhage (P = 0.04), hypertension (P = 0.04), initial HD (P = 0.04), and sclerotic class (P = 0.004) were associated with ESRD. In our patients, a sclerotic class was associated with a higher risk of ESRD, suggesting that histo- pathological classification is potentially an important parameter to predict outcomes in renal disease secondary to ANCA-associated vasculitis.

How to cite this article:
Jebali H, Khadhar M, Mami I, Beji S, Sellami M, Hassen M, Hmida FB, Chermiti M, Ghabi H, Salem TB, Houman H, Raies L, Zouaghi MK. Predictors of renal outcomes in anti-neutrophil cytoplasmic antibody glomerulonephritis. Saudi J Kidney Dis Transpl 2020;31:182-90

How to cite this URL:
Jebali H, Khadhar M, Mami I, Beji S, Sellami M, Hassen M, Hmida FB, Chermiti M, Ghabi H, Salem TB, Houman H, Raies L, Zouaghi MK. Predictors of renal outcomes in anti-neutrophil cytoplasmic antibody glomerulonephritis. Saudi J Kidney Dis Transpl [serial online] 2020 [cited 2020 Apr 7];31:182-90. Available from: http://www.sjkdt.org/text.asp?2020/31/1/182/279939



   Introduction Top


Anti-neutrophil cytoplasmic antibody (ANCA)- associated vasculitis (AAV) is a heterogeneous group of inflammatory diseases that affects the small vasculatures in multiple organs, but primarily the kidneys. Histopathologically, the typical renal involvement in AAV is characterized by pauci-immune necrotizing and cre- scentic glomerulonephritis.The diversity of the histopathologic findings ranges from fresh fibrinoid necrosis with cellular crescents to global sclerosis.[1] In addition to its diagnostic value, renal histological study has a therapeutic and prognostic impact as well. Thus, a classification proposed by Berden et al in 2010 separates biopsies into four classes: focal, crescentic, mixed, and sclerotic, and it was initially shown that these categories predicted renal outcome.[2] The prognostic value of this histopathologic classification has been evaluated throughout the world. A meta-analysis showed that patients with focal class had the best outcome, while the sclerotic class had the worst.[3] Recently, Brix et al proposed a clinically applicable renal risk score that allowed early risk prediction of end-stage renal disease (ESRD).[4] In the present study, we analyzed clinical and histological findings of 37 patients with ANCA-associated glomerulonephritis and assessed the prognostic impact of glomerular classification and renal risk score on renal survival in our population.


   Patients and Methods Top


Thirty-seven patients with AAV with histolo- gically-proven renal injury were studied retrospectively over a period of nine years. These patients were referred to the nephrology department between June 2007 and March 2016 either for exploration of pulmonary renal syndrome or acute renal failure and/or rapidly progressive glomerulonephritis. The diagnosis of AAV was made based on the Chapel Hill consensus.[5] Only patients with histologically confirmed renal disease were included in our study. Patients were excluded if they had secondary vasculitis. The renal survival, defined as time to develop ESRD requiring dialysis initiation, was evaluated based on clinical parameters, the histopathological classification,[3] and renal risk score.[4]

Anti-neutrophil cytoplasmic antibody analysis

All patients had been tested for the presence of ANCA by indirect immunofluorescence. Enzyme-linked immunosorbent assay was performed to test for anti-myeloperoxidase (MPO) and anti-proteinase 3 (PR3) antibodies in all sera.

Histological study

Renal specimens were evaluated using light microscopy with direct immunofluorescence staining for immunoglobulins and complement components. The biopsy specimens were assigned to four categories according to the definition of the 2010 histological classifi- cation.[3] Tubulointerstitial lesions such as interstitial fibrosis and tubular atrophy and interstitial inflammation were graded semi- quantitatively (1 for <25%, 2 for >25% and <50%, and 3 for >50%). Arteritis was scored as present or absent.

Definitions

Glomerular filtration rate (GFR) was estimated according to the Modification of Diet in Renal Disease formula.[6] Disease activity was scored using the Birmingham Vasculitis Activity Score (BVAS), 2003.[7]

Complete remission: normalization of renal function and disappearance of urinary sediment abnormalities associated with the resolution of extra-renal manifestations.

Partial remission: an improvement without normalization of the renal function and/or stabilization of the renal function as well as the resolution of extra-renal manifestations.

Relapse: A reactivation of the disease following a remission. It can manifest as a rapid deterioration of renal function associated with abnormal urinary sedimentation and/or worsening or onset of new extra-renal signs.

ESRD: creatinine clearance <10 mL/min/1.73 m2 and/or the use of chronic renal replacement therapy.

The renal risk score:[4] it is a score including three parameters:

Percentage of normal glomeruli (N) : N0 >25%, N1 10%-25%, N2 <10%. Percentage of interstitial fibrosis and tubular atrophy (T): T0 ≤25%, T1 >25%. GFR at the time of diagnosis (G): G0 ≤15 mL/min/1.73 m2, G1 <15 mL/min/1.73 m2. N1: 4 points, N2: 6 points, T1: 2 points, G1:3 points.

The resulting score was used to classify predicted ESRD risk at 36 months as low (0 point: 0%), intermediate (2-7 points: 26 %), or high (8-11 points: 68%-78%).


   Statistical Analysis Top


The data were analyzed using IBM SPSS Statistics software version 20.0 (IBM Corp., Armonk, NY, USA). We calculated simple frequencies and relative frequencies (percentages) for qualitative variables. We calculated also the means, medians, standard deviations, and determined the extreme values for the quantitative variables. Survival data were studied by establishing a survival curve according to the Kaplan-Meier method. The determination of prognostic factors of survival was performed in univariate analysis by comparing the survival curves with the Log-rank test (P<0.05).


   Results Top


We enrolled 37 patients with ANCA-associated glomerulonephritis, including 22 with microscopic polyangiitis (MPA) and 15 with granulomatosis and polyangiitis (GPA). The median age at the time of the diagnosis was 54 ± 16 years (17-80 years). Our study included 19 women and 18 men with a sex ratio of 0.94. Anti-MPO antibodies were positive in 22 cases (59.4%) and anti-PR3 antibodies were identified in 15 (40.6%). All patients with GPA had anti-PR3 antibody, and all patients with MPA had anti-MPO antibody. The average BVAS score was 23 ± 8 (9-41). Lungs, upper respiratory tract and neurological involvement were the most common extrarenal manifestations at diagnosis [Table 1].
Table 1: Extra-renal manifestations seen in our study patients.

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Regarding renal manifestations, oligo-anuria was noted in 15 patients (40.5%) and six patients (21.6%) had hypertension. Mean baseline serum creatinine (SCr) was 6.3 mg/dL (0.9-16.1 mg/dL). Mean Cr clearance was 16.7 mL/min/1.73 m2 (3-93). Thirty-five patients (94.5%) had renal failure at presentation. Eight patients (21.6%) had nephrotic syndrome [Table 2].
Table 2: Renal involvement, clinical characteristics, and renal risk score of the patients among four histological classes.

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In this cohort, patients had a median of 21 glomeruli per biopsy specimen. A detailed histologic analysis of biopsies was performed. [Table 3] illustrates findings of glomerular, tubulointerstitial, and vascular lesions. We noted a predominance of the sclerotic class. The immunofluorescence staining revealed pauci-immune glomerulonephritis in all cases.
Table 3: Histological lesions of the study patients.

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All patients were treated with corticosteroids in combination with cyclophosphamide (CYC) for induction therapy. Glucocorticoids were administered initially intravenous (IV) at a dose of 15 mg/kg/day of methylprednisolone daily for three days, followed by oral corticosteroids (prednisone) at a dose of 1 mg/kg/day with progressive taper. CYC (Endoxan®) was administered as an IV pulse in all patients. Seventeen patients received monthly pulses, 12 patients received bimonthly pulses, and eight patients received the first three pulses at 15-day intervals and three patients at 21-day intervals. Plasma exchanges were performed in five patients. Initial hemodialysis (HD) was indicated in 23 patients (61.1%). The maintenance treatment was with azathioprine in 19 cases (95%) and mycophenolate mofetil in one case (5%). Seventeen patients did not receive maintenance treatment because of a death in five cases, ESRD in eight patients and a loss of follow-up in four cases.

The median follow-up period was 33.15 ± 22 months (1-145 months). Complete remission was noted in six cases (17.6%) and partial remission in 14 (41.2%). Relapses were noted in five cases after an average of 10.6 months. Six patients died. Seventeen patients (43.2%) developed ESRD [Figure 1] after an average delay of 6.5 months (a few days-48 months). Among patients who required initial HD, only seven patients recovered renal function. Regarding renal risk score, we had five patients (13.5%) with low risk, 17 with intermediate risk (45.9%), and 15 (40.6%) with high risk. ESRD was occurred in 47% (8 patients) of intermediate-risk group and 66% (10 patients) of high-risk group.
Figure 1: Renal survival in the study patients.

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In our study, we found, at univariate analysis, that the following factors were significantly associated with the occurrence of ESRD: smoking (P = 0.02), alveolar hemorrhage (P = 0.04), hypertension (P = 0.04), initial HD (P = 0.04), and sclerotic class (P = 0.004). Age, proteinuria, renal failure at presentation, BVAS score, RRS, relapses, and tubulointerstitial involvement had no influence on renal prognosis.


   Discussion Top


Through this study, we tried to specify the characteristics of renal involvement and to determine the factors influencing the renal prognosis. The study included cases with severe renal involvement. Indeed, 61% of our patients required HD initially. Histologically, we noted a predominance of the sclerotic class. Despite treatment, ESRD occurred in 43.2% of cases. Renal involvement in AAV is frequent, ranging from 80% to 97% according to various studies.[8],[9],[10],[11] It is seen in 70% of cases of GPA and almost 100% of cases of MPA.[12],[13] It conditions the renal and vital prognosis as well.[14] Thus, the degree of the severity of this disease is one of the pillars to be considered in the therapeutic decision.

Regarding extra-renal manifestations, the lung was the most frequently affected organ.[15],[16] Alveolar hemorrhage was noted in 64.7% of patients with GPA and 50% of cases with MPA, far exceeding the data in the literature, wherein an average of 40% of patients presented with alveolar hemorrhage.[15]

According to the most reported series, renal failure is noted on an average in 50%-60% of cases.[10],[11],[17],[18] In our population, 95% of cases had renal failure when the renal biopsy was performed and 61% of patients required initial HD. This confirms the severity of the initial picture in our patients. According to EUVAS classification, we noted the predominance of sclerotic class unlike the data in the literature.[3],[19]

The frequency of occurrence of ESRD is variously reported in the literature. Its frequency varies according to the study period, the clinical and histological features of kidney disease and the therapeutic protocols. It ranges between 20% and 50%.[20],[21],[22],[23],[24],[25],[26],[27],[28] In our study, 43.2% of our patients reached ESRD after an average period of 6% months. Even by homogenizing treatment and duration of follow-up, the evolution of renal function during AAV remains rather unpredictable. As a result, the analysis of prognostic factors has attracted the interest of several authors. The main prognostic factors that can influence the evolution toward ESRD, described in some studies are summarized in [Table 4]. Initial SCr and initial HD were the main clinical prognostic determinants.[29],[30],[31] In our study, only initial HD was associated with the occurrence of ESRD. This would be related to the limited number of patients and the almost constant presence of the deterioration of renal function in our patients. The impact of tobacco on AAV expression and evolution is not well known. Benarous et al have noted that renal involvement is less common in patients who smoke.[32] Haubitz et al found no impact of smoking on renal function or mortality.[33] In our study, however, smoking was significantly associated with progression to ESRD.
Table 4: Literature review: Prognostic factors of renal disease.

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The prognostic value of renal biopsy is widely known in patients with AAV because specific renal pathologic lesions, either absence or presence, are important factors in predicting renal outcome. Several studies have already suggested that the percentage of normal glomeruli is a reliable predictor.[22] Bajema et al demonstrated that in ANCA-associated renal vasculitis, the proportion of normal glomeruli rather than the number of active lesions, was a reliable predictor of renal function during follow-up.[34],[35] Both chronic and acute tubulo- interstitial lesions were negatively correlated with renal function at one-year after diagnosis in patients with severe renal involvement.[36] In our study, tubulo-interstitial injury was not associated with renal outcome. In recent years, Berden et al have proposed a classification based on glomerular lesions as the new histopathological classification for ANCA- associated glomerulonephritis.[2] Multivariate analysis showed that histopathological classes and baseline renal function were the only significant independent predictors of renal function at 1- and 5-year follow-up.[2] Histological classes, in the order of focal, crescentic, mixed, and sclerotic, were associated with an increasing risk of developing ESRD during follow-up. The focal class would have the best prognosis and the sclerotic class presents the greatest risk of progression to ESRD.[17],[19] For the mixed class and the cre- scentic class, the prognosis varies according to various studies. A recent meta-analysis involving >1500 patients could not detect different outcomes in the crescentic and mixed classes.[3] In our study, only the sclerotic class was associated with progression to ESRD. Given the limited number of patients in the other classes, we did not identify the prognostic impact of these factors. Recently, Brix et al proposed a clinically applicable renal risk score for ANCA-associated GN. This score predicted ESRD at 36 months.[4] It included estimated GFR, the percentage of normal glomeruli and the percentage of interstitial fibrosis and tubular atrophy. Patients are subdivided into three groups: low risk, intermediate risk, and high-risk. We found that regarding RRS, patients with intermediate risk had a worse prognosis than in the Brix et al cohort. The renal risk score is a simple method for predicting renal prognosis in ANCA- associated vasculitis, but it needs to be validated in different studies before it can be applied to clinical practice broadly.

Our series is limited by the fact that it is retrospective, concerns a small population and monocentric. Our main goal was to determine the renal prognosis during the evolution but we have a selection bias as the recruitment was made in a nephrology department where the kidney involvement was in the first line. These data deserve to be confirmed by a multicenter prospective study with a greater number of patients.


   Conclusion Top


The prognosis of AAV remains poor, dominated by pulmonary and renal complications. Rapid and urgent management is needed to administer appropriate treatment and avoid progression to renal fibrosis. The kidney is the organ most frequently affected during AAV, thus worsening the prognosis of the disease. Knowledge of the prognostic factors will help optimize the therapeutic management.

Conflict of interest: None declared.



 
   References Top

1.
Berden AE, WesterTrejo MAC, BajemaIM. Investigations in systemic vasculitis - The role of renal pathology. Best Pract Res Clin Rheumatol 2018;32:83-93.  Back to cited text no. 1
    
2.
Berden AE, Ferrario F, Hagen EC, et al. Histopathologic classification of ANCA-asso- ciated glomerulonephritis. J Am Soc Nephrol 2010;21:1628-36.  Back to cited text no. 2
    
3.
Chen YX, Xu J, Pan XX, et al. Histo- pathological classification and renal outcome in patients with antineutrophil cytoplasmic antibodies-associated renal vasculitis: A study of 186 patients and metaanalysis. J Rheumatol 2017;44:304-13.  Back to cited text no. 3
    
4.
Brix SR, Noriega M, Tennstedt P, et al. Development and validation of a renal risk score in ANCA-associated glomerulonephritis. Kidney Int 2018;94:1177-88.  Back to cited text no. 4
    
5.
Jennette JC, Falk RJ, Bacon PA, et al. 2012 revised international Chapel Hill consensus conference nomenclature of vasculitides. Arthritis Rheum 2013;65:1-1.  Back to cited text no. 5
    
6.
KDIGO2012. Clinical practice guideline for the evaluation and management of chronic kidney disease. Kidney Int 2013;3:1-150.  Back to cited text no. 6
    
7.
Mukhtyar C, Lee R, Brown D, et al. Modification and validation of the Birmingham vasculitis activity score (version 3). Ann Rheum Dis 2009;68:1827-32.  Back to cited text no. 7
    
8.
Seo P, Stone JH. The antineutrophil cyto- plasmic antibody-associated vasculitides. Am J Med 2004;117:39-50.  Back to cited text no. 8
    
9.
Fauci AS, Haynes BF, Katz P, Wolff SM. Wegener’s granulomatosis: Prospective clinical and therapeutic experience with 85 patients for 21 years. Ann Intern Med 1983;98:76-85.  Back to cited text no. 9
    
10.
Rahmattulla C, de Lind van Wijngaarden RA, Berden AE, et al. Renal function and ear, nose, throat involvement in anti-neutrophil cytoplasmic antibody-associated vasculitis: Prospective data from the European Vasculitis Society clinical trials. Rheumatology (Oxford) 2015;54:899-907.  Back to cited text no. 10
    
11.
Frausová D, Hrušková Z, Lánská V, Lachmanová J, Tesař V. Long-term outcome of patients with ANCA-associated vasculitis treated with plasma exchange: A retrospective, single-centre study. Arthritis Res Ther 2016;18:168.  Back to cited text no. 11
    
12.
Schilder AM. Wegener’s granulomatosis vas- culitis and granuloma. Autoimmun Rev 2010; 9:483-7.  Back to cited text no. 12
    
13.
Villiger PM, Guillevin L. Microscopic polyangiitis: Clinical presentation. Autoimmun Rev 2010;9:812-9.  Back to cited text no. 13
    
14.
Flossmann O, Berden A, deGroot K, et al. Long-term patient survival in ANCA- associated vasculitis. Ann Rheum Dis 2011; 70:488-94.  Back to cited text no. 14
    
15.
Andreiana I, Stancu S, Avram A, Taran L, Mircescu G. ANCA positive crescentic glomerulonephritis outcome in a Central East European cohort: A retrospective study.BMC Nephrol 2015;16:90.  Back to cited text no. 15
    
16.
Hruskova Z, Casian AL, Konopasek P, et al. Long-term outcome of severe alveolar haemorrhage in ANCA-associated vasculitis: A retrospective cohort study. Scand J Rheumatol 2013;42:211-4.  Back to cited text no. 16
    
17.
Córdova-Sánchez BM, Mejía-Vilet JM, Morales-Buenrostro LE, Loyola-Rodríguez G, Uribe-Uribe NO, Correa-Rotter R. Clinical presentation and outcome prediction of clinical, serological, and histopathological classification schemes in ANCA-associated vasculitis with renal involvement. Clin Rheumatol 2016;35:1805-16.  Back to cited text no. 17
    
18.
Westman K, Flossmann O, Gregorini G. The long-term outcomes of systemic vasculitis. Nephrol Dial Transplant 2015;30Suppl 1:i60- 6.  Back to cited text no. 18
    
19.
Tanna A, Guarino L, Tam FW, et al. Longterm outcome of anti-neutrophil cytoplasm antibody-associated glomerulonephritis: Evaluation of the international histological classification and other prognostic factors. Nephrol Dial Transplant 2015;30:1185-92.  Back to cited text no. 19
    
20.
Chang DY, Wu LH, Liu G, Chen M, Kallenberg CG, Zhao MH. Re-evaluation of the histopathologic classification of ANCA- associated glomerulonephritis: A study of 121 patients in a single center. Nephrol Dial Transplant 2012;27:2343-9.  Back to cited text no. 20
    
21.
Hogan SL, Nachman PH, Wilkman AS, Jennette JC, Falk RJ. Prognostic markers in patients with antineutrophil cytoplasmic auto- antibody-associated microscopic polyangiitis and glomerulonephritis. J Am Soc Nephrol 1996;7:23-32.  Back to cited text no. 21
    
22.
Andrassy K, Erb A, Koderisch J, Waldherr R, Ritz E. Wegener’s granulomatosis with renal involvement: Patient survival and correlations between initial renal function, renal histology, therapy and renal outcome. Clin Nephrol 1991; 35:139-47.  Back to cited text no. 22
    
23.
Aasarød K, Iversen BM, Hammerstrøm J, Bostad L, Vatten L, Jørstad S. Wegener’s granulomatosis: Clinical course in 108 patients with renal involvement. Nephrol Dial Transplant 2000;15:611-8.  Back to cited text no. 23
    
24.
Lionaki S, Hogan SL, Jennette CE, et al. The clinical course of ANCA small-vessel vas- culitis on chronic dialysis. Kidney Int 2009; 76:644-51.  Back to cited text no. 24
    
25.
Rhee RL, Hogan SL, Poulton CJ, et al. Trends in long-term outcomes among patients with antineutrophil cytoplasmic antibody-associated vasculitis with renal disease. Arthritis Rheumatol 2016;68:1711-20.  Back to cited text no. 25
    
26.
Chang DY, Luo H, Zhou XJ, Chen M, Zhao MH. Association of HLA genes with clinical outcomes of ANCA-associated vasculitis. Clin J Am Soc Nephrol 2012;7:1293-9.  Back to cited text no. 26
    
27.
Li ZY, Gou SJ, Chen M, Zhao MH. Predictors for outcomes in patients with severe ANCA- associated glomerulonephritis who were dialysis-dependent at presentation: A study of 89 cases in a single Chinese center. Semin Arthritis Rheum 2013;42:515-21.  Back to cited text no. 27
    
28.
Lee T, Gasim A, Derebail VK, et al. Predictors of treatment outcomes in ANCA-associated vasculitis with severe kidney failure. Clin J Am SocNephrol 2014;9:905-13.  Back to cited text no. 28
    
29.
Franssen CF, Gans RO, Arends B, et al. Differences between anti-myeloperoxidase- and anti-proteinase 3-associated renal disease. Kidney Int 1995;47:193-9.  Back to cited text no. 29
    
30.
Bligny D, Mahr A, Toumelin PL, Mouthon L, Guillevin L. Predicting mortality in systemic Wegener’s granulomatosis: A survival analysis based on 93 patients. Arthritis Rheum 2004;51:83-91.  Back to cited text no. 30
    
31.
HarperL, Savage CO. ANCA-associated renal vasculitis at the end of the twentieth century— a disease of older patients. Rheumatology (Oxford) 2005;44:495-501.  Back to cited text no. 31
    
32.
Benarous L, Terrier B, Puécha lX, et al. Tobacco differentially affects the clinical- biological phenotypes of ANCA-associated vasculitides. Clin Exp Rheumatol 2015;33:S- 116-21.  Back to cited text no. 32
    
33.
Haubitz M, Woywodt A, deGroot K, Haller H, Goebel U. Smoking habits in patients diagnosed with ANCA associated small vessel vasculitis.Ann Rheum Dis 2005;64:1500-2.  Back to cited text no. 33
    
34.
Bajema IM, Hagen EC, Hansen BE, et al. The renal histopathology in systemic vasculitis: An international survey study of inter- and intra- observer agreement. Nephrol Dial Transplant 1996;11:1989-95.  Back to cited text no. 34
    
35.
Bajema IM, Hagen EC, Hermans J, et al. Kidney biopsy as a predictor for renal outcome in ANCA-associated necrotizing glomerulo- nephritis. Kidney Int 1999;56:1751-8.  Back to cited text no. 35
    
36.
de Lind van Wijngaarden RA, Hauer HA, Wolterbeek R, et al. Clinical and histologic determinants of renal outcome in ANCA- associated vasculitis: A prospective analysis of 100 patients with severe renal involvement. J Am SocNephrol 2006;17:2264-74.  Back to cited text no. 36
    

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Correspondence Address:
Hela Jebali
Department of Nephrology, Dialysis and Transplantation, La Rabta Hospital, Tunis
Tunisia
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DOI: 10.4103/1319-2442.279939

PMID: 32129212

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