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Year : 2007  |  Volume : 17  |  Issue : 2  |  Page : 53-60

Study of renal histopathological correlation with anticardiolipin antibody status in patients with systemic lupus erythematosus

Department of Medicine, KEM Hospital and Seth GS Medical College, Parel, Mumbai, India

Correspondence Address:
Ramshekhar N Menon
Department of Medicine, KEM Hospital and Seth GS Medical College, Parel, Mumbai - 400 012
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0971-4065.37021

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Background: Detection of antiphospholipid antibodies in patients with lupus nephritis is useful not only to identify patients at a risk for vascular and obstetric manifestations but also for their potential deleterious impact on renal outcome. Materials and Methods: 50 patients who met the American Rheumatology Association criteria for systemic lupus erythematosus (SLE) and (under suspicion of lupus nephritis) qualified for renal biopsy were enrolled into this observational study. In addition to the standard protocol of investigations in SLE, anticardiolipin antibody (aCL) status was determined during the initial workup and was confirmed after 6 weeks. Renal biopsy was studied by a senior experienced pathologist. In addition to the WHO class discrete histological markers of morbidity such as capillary thickening, hyaline thrombi, crescent and wire-loop formation, interstitial fibrosis and tubular atrophy were studied. Hypocomplementemia, urine analysis and renal function tests were also compared between aCL+ and aCL- patients. Results: 58% of the patients were aCL+ according to a standard ELISA estimation. Antiphospholipid Syndrome Nephropathy (APSN) was detected in 4 out of 28 aCL+ patients ( P = 0.4). There was no difference in the SLE Disease Activity Index (SLEDAI) scores between the two groups. There was evidence of persistent hypocomplementemia (C3 or C3 and C4) at the end of 6 months on therapy in aCL+ patients. ( P = 0.008). This significance was not attained in terms of azotemia, active urinary sediments or proteinuria. There was no difference in WHO (or RPS) class prevalence and calculated activity and chronicity scores. However, there was a greater incidence of capillary thickening ( P = 0.08), interstitial fibrosis ( P = 0.019) and tubular atrophy ( P = 0.052) in aCL+ patients as opposed to the quantitative score assessment using the activity and chronicity indices. Conclusions: Hypocomplementemia is the only probable marker of renal morbidity in the laboratory follow-up of the SLE patients. aCL positivity does contribute to greater incidence of interstitial fibrosis, tubular atrophy and capillary wall thickening in biopsy specimens. APSN is an independent entity that must be specifically sought for on histological assessment.

Keywords: Systemic lupus erythematosus, antiphospholipid syndrome nephropathy, antiphospholipid antibody

How to cite this article:
Menon RN, Bichile L S. Study of renal histopathological correlation with anticardiolipin antibody status in patients with systemic lupus erythematosus. Indian J Nephrol 2007;17:53-60

How to cite this URL:
Menon RN, Bichile L S. Study of renal histopathological correlation with anticardiolipin antibody status in patients with systemic lupus erythematosus. Indian J Nephrol [serial online] 2007 [cited 2022 Nov 26];17:53-60. Available from:

  Introduction Top

Anticardiolipin antibody status predisposes to vascular thrombosis in many systems in the setting of the already morbid patient with systemic lupus erythematosus (SLE). The renal manifestations of the antiphospholipid antibody syndrome (APS) are heralded by a thrombotic microangiopathy with acute and chronic manifestations that contribute to renal morbidity. This study attempts to gain an insight into what anticardiolipin antibody (aCL) status does to lupus nephritis in terms of renal function and renal histology.

  Materials and Methods Top

Fifty newly diagnosed patients of either sex between the ages of 15-55 who met the American Rheumatology Association (ARA) criteria for SLE and satisfied the criteria for renal biopsy were randomly selected from medicine/rheumatology OPD or medicine wards. In addition to the internationally recommended investigations, the defining investigations in our study were anticardiolipin antibody (IgG and IgM aCL in units/ml) estimation and renal biopsy. The aCL estimation was performed by a standard ELISA for beta-2-glycoprotein 1-dependent anticardiolipin antibodies. aCL titers were standardized to age- and sex-matched population controls. The follow-up investigations were repeated at 3 months, 6 months and 1 year (between January 2004 and July 2005). Lupus anticoagulant could not be estimated due to technical reasons.

In addition to the clinical profile of SLE, the aCL manifestations were studied as per the Sapporo criteria for primary APS [1] and the Alarcon-Segovia criteria (1992) for APS in the patients with SLE. [2]

Patients were divided into two groups: aCL negative (two values 6 weeks apart, which were <2SD from control) and aCL positive patients. All these patients were further followed up as per the investigation protocol. All the patients with SLE, irrespective of the aCL status, were biopsied on the evidence of proteinuria >500 mg/24 h with an evidence of hypocomplementemia or active urine sediments. The category of lupus nephritis was assessed by a senior pathologist (using light microscopy) as per the WHO criteria. The involvement secondary to APS (Antiphospholipid Syndrome Nephropathy - APSN) was studied in the renal biopsies.

All patients received standard WHO recommended therapy (antimalarials, steroids with or without cyclophosphamide). aCL positive patients with thrombotic manifestations, including APSN, received vasoprotective therapy with aspirin and warfarin titrated to international normalized ratio (INR) of 2-3 for 6 months and 1.5-2 thereafter.

Patients with persistent proteinuria >500 mg/day, active urine sediments or abnormal renal function tests at the end of 1 year of the standard therapy were biopsied to establish the nature of histological progression.

Observations and results were tabulated and interpreted by a statistical analysis. Various tests of significance were applied. Chi-square test was used to compare the qualitative data, and the t-tests were used to compare the quantitative data. A P value of <0.05 was considered significant.

  Results Top

Data from 48 patients were evaluated as 2 patients did not follow-up. The mean age of our cohort was 24.8 ±8 years; Only 3 males were studied. The mean age of presentation in them was 26.4 years. [Table - 1] shows an aCL positivity of 58.3%. As far as the SLE disease activity scores are concerned between the two groups, the difference was not statistically significant except for a mean higher SLE Disease Activity Index (SLEDAI) score in aCL+ group (39.6 vs 33.5; P = 0.069).

There was no significant difference between the blood urea levels ( P = 0.155) or creatinine levels ( P = 0.189) under comparison except for the fact that more patients in the aCL+ group had raised levels (azotemia). This difference was nonexistent at the end of the follow-up on therapy ( P = 0.793 and 0.345, respectively)

There was also no difference in the incidence of active sediments in urine or qualitative albuminuria between the two groups ( P = 0.46 and 0.80 at initial and annual assessments, respectively).

There was also no difference observed between the two groups in the quantitative 24-h proteinuria estimation at the initial and 1 year follow-up ( P = 0.8); however, at 6 months, aCL+ patients had a higher incidence of proteinuria ( P = 0.1).

An important inflammatory marker studied was the erythrocyte sedimentation rate (ESR). There was no significant difference in the mean values between the two groups ( P = 0.24) with a slightly higher ESR among the aCL+ patients.

Studying the pattern of hypocomplementemia revealed some interesting trends. C3 and C4 were low in 82.1% of aCL+ patients and 65% of aCL- patients, and the exclusive C3 values decreased in 30% of aCL- patients and 7.1% of aCL+ patients. ( P = 0.102). Incidence of persistent hypocomplementemia at 3 months (C3 or both C3, C4) showed no difference between the two groups. However at 6 months, 35.7% of aCL+ patients showed a decrease in both C3 and C4 as opposed to 10% of aCL-. 42.9 % of aCL+ patients demonstrated a persistent C3 hypocomplementemia as opposed to 25% of aCL- ( P = 0.008). However, at 1 year, 50% of aCL+ and 60% of aCL- patients had normalization of the complements and the incidence of persistent hypocomplementemia between the two groups was not significant (28.6% vs 15%; P = 0.541) [Table - 2],[Table - 3],[Table - 4],[Table - 5].

This is in good agreement with our trends in proteinuria, although the results on the complements was significant

Hence, there was considerable difference in persistent hypocomplementemia (amounting to greater clinical morbidity as quoted by previous studies; vide infra ) at 6 months (χ2 = 9.732, P = 0.008) with an insignificant but evident difference from that at the initiation of therapy.

The features on renal histology were examined individually depending on the renal class (WHO and ISN/RPS), activity and chronicity indices. Patients who were subjected to repeat biopsy at the end of 1 year of therapy were separately considered. A statistically non-significant greater number of aCL+ patients require repeat renal biopsy.

Fifty percent of aCL- and 50% of aCL+ had class II lupus nephritis. Twenty percent of aCL- and 28.6% of aCL+ had features of class IV (A). The features of class IV(A/C) was found in 7.1% of aCL+ patients. Only 1 aCL+ patient exhibited the features of class IV(C). Ten percent of aCL- and 3.6% of aCL+ had features of both class IV and V. Fifteen percent of aCL- and 7.1% of aCL+ exhibited class V histology. These differences were not statistically significant (Chi square = 6.446; P = 0.597).

Repeat biopsy was required in one aCL- patient and six aCL+ patients on account of persistent significant proteinuria. In the aCL- group, the patient had class IV(A) lupus nephritis.

In the aCL+ group, two of the six patients had initial APSN along with their respective class IV(A) and class IV(A/C). Repeat biopsy revealed class II in the first and IV(A/C) in the other. The remaining 4 biopsies showed persistence of either class IV(A) or class IV(A/C). These results were also insignificant ( P = 0.494).

Renal biopsies that were performed at the end of more than 1 year of therapy revealed no difference in the activity indices on initial assessments or repeat biopsies ( P = 0.882 and 0.778). The same trend was observed for the chronicity indices ( P = 0.24 and 0.734, respectively). Thus, aCL positivity had no correlation whatsoever with the class of renal lupus. Hence, aCL positivity does not contribute to increased histological morbidity in renal lupus. The main histological derivant of aCL positivity was the presence of APSN [Figure - 1],[Figure - 2].

Description of acute features of APSN as seen in [Figure - 2].

a) Glomeruli show variable increase in mesangial matrix.

b) Patchy thickening of glomerular capillary walls with the formation of occasional wireloops.

c) Two to four glomeruli show "double contour" appearance of capillary walls and "fluffy" appearance of the glomerular mesangium specific to APSN.

d) One glomerular capillary contains fibrinous material in its lumen; another change secondary to antiphospholipid antibody.

e) Karyorhectic debris is observed in the glomerulus. Hyaline granular casts are observed in the lumen of few tubules and interstitium shows focus of infiltration by lymphocytes and few neutrophils.

[Table - 6] shows the acute and chronic histological manifestations of APSN. [3]

Histopath slide (40x magnification) shows the postmortem specimen slide of primary antiphospholipid syndrome. A large intra renal artery is stained with elastin. Classical thrombotic microangiopathy is observed with the splitting of internal elastic lamina, endothelial edema and degeneration. Large hyaline-organized thrombi occlude the lumen.

Thus, only 8.3% of the total biopsy specimens (14.2% of aCL+ patients) revealed the entity called APSN. This is a very small number to be statistically significant, and the evaluation of a larger series is required in order to comment on its incidence. Two of these patients were class II lupus, one patient had class IV(A) lupus and one had class IV(A/C). Repeat biopsy was required in only two patients with acute features of APSN due to proteinuria; one showed a shift to class II and another persisted in class IV(A/C). Those with chronic features in the form of focal cortical and ischemic atrophy had nephrotic range proteinuria. Hypertension was observed in two out of these four patients; two out of four had seizures. One patient had recurrent abortions (second trimester), and one had autoimmune hemolytic anemia and thrombocytopenia. Azotemia was observed in two patients at the time of initial biopsy. All the four patients demonstrated clinical improvement on therapy and oral anticoagulation. Thus, APSN was concluded to be an independent entity that may not have an ideal correlation with aCL positivity. Details on individual patients are as follows:

Patient 1: 15-year-old female; (aCL IgG and M > 5 Standard Deviations {SD} of control); class IV(A) lupus nephritis-activity index = 9, chronicity index = 0; presented with autoimmune hemolytic anemia and immune thrombocytopenia. Renal function was normal. Histology [Figure - 3] revealed acute changes in the APSN ("double contour" appearance of capillary walls and "fluffy" appearance of glomerular mesangium with evidence of fibrinous material in one capillary lumen). She required repeat biopsy on account of persistent proteinuria. Biopsy showed the resolution of changes in the APSN [Figure - 2] and class IIb nephritis. She was treated with prednisolone and cyclophosphamide. Once the hematological parameters normalized, she was administered aspirin and warfarin. There was one episode of menorrhagia after 6 months due to warfarin toxicity. After indoor treatment, she was continued on low-intensity anticoagulation.

Patient 2: 19-year-old female; (aCL IgG > 5 SD, IgM 2-5SD); presented with nephritic syndrome; normal renal function tests. Histology revealed class II lupus nephritis with focal cortical atrophy [Figure - 1], a feature of chronic APSN. She responded to steroids and warfarin and aspirin.

Patient 3: 22-year-old female; (aCL IgG < 2 SD, IgM 2-5 SD); history of two first trimester abortions. Presented with malignant hypertension (hypertensive encephalopathy, microangiopathic hemolytic anemia, and azotemia). Incidentally, she was ANCA positive on serology. Histology revealed class II lupus nephritis with ischemic obsolescence, specific to APSN, and tubular atrophy. She was started on steroids, warfarin and antihypertensives.

Patient 4: 26-year-old female; (aCL IgG and M 2-5 SD); history of seizures and psychosis with azotemia and hypertension. Class IV(A/C) lupus nephritis with activity index = 4, chronicity index = 1. The evidences of ischemic atrophy, endothelial swelling, tuft retraction and one intraglomerular thrombus was observed. Repeat biopsy required on account of persistent proteinuria revealed the same class of nephritis and the same chronic changes of APSN. She was started on steroids and cyclophosphamide and warfarin and aspirin.

The differences in terms of various histological features were studied again in relation to individual aspects of aCL positivity. In the study of all biopsy specimens, hyaline thrombi were detected in 18% of aCL+ and 15% of aCL-. However, capillary wall thickening was demonstrated in 50% of aCL+ as opposed to 25% of aCL- patients ( P = 0.08). There was no significant difference between the 2 groups in the incidence of crescents or wire loops ( P = 0.130). There was also no significant difference between the two groups in the incidence of mesangial proliferation (observed in all the biopsy samples), global or segmental sclerosis ( P = 0.386). However, the significant finding is in the greater incidence of both interstitial fibrosis and tubular atrophy in aCL+ patients ( P = 0.019 and 0.052, respectively) [Figure - 4],[Figure - 5],[Figure - 6],[Figure - 7],[Figure - 8].

  Discussion Top

Of the 50 patients enrolled for the study, two were lost to follow-up; hence, 48 patients were evaluated. In the cohort of these 48 patients under study, 58% were aCL positive and 42% were aCL negative. The incidence of aCL in various studies of SLE is anywhere between 30-63%. A study by Fofi et al. revealed 40.2% incidence. [4] Naiker et al. revealed an incidence of 45%. [5] All the patients were followed up on various clinical and laboratory parameters, as mentioned above. Ghirardello et al. found that 51.4% of SLE patients were positive for aCL and 8.6% were positive for lupus anticoagulant, whilst in a retrospective study by Horbach, IgG aCL were found in 64% of patients with a history of thrombosis and 41% in those without thrombosis. [6]

In the aCL- group, three out of 10 class II patients, and 2/5 class IV patients and 2/5 class V patients showed a decrease in either C3 or both C3 and C4. In aCL+ patients, 11/14 class II patients and 7/11 class IV and 2/3 class V lupus exhibited the same trend ( P = 0.04). Hence, persistent hypocomplementemia into therapy could indicate a greater renal clinical morbidity as well as delayed response to the therapy in aCL+ patients. In a 10-year retrospective study of 597 SLE patients and 70 patients with primary antiphospholipid antibody syndrome by Ramos-Casals et al. , it was concluded that those with hypocomplementemia showed a higher prevalence of female gender ( P < 0.001), fever ( P = 0.021), nephropathy ( P < 0.001), cutaneous vasculitis ( P = 0.023), positive anti-dsDNA antibodies ( P = 0.012) and cryoglobulinemia ( P < 0.001). In addition, patients with hypocomplementemia showed a higher prevalence of APS-related features such as hemolytic anemia ( P = 0.001) and antiphospholipid antibodies ( P < 0.001). Hypocomplementemia was prospectively related to accumulated hospitalization in SLE patients, but not with the accumulated number of lupus flares or with the survival after a follow-up of five years. In contrast, 33 (47%) patients with primary APS presented low complement values, which were associated with a higher prevalence of livedo reticularis ( P = 0.022), thrombocytopenia ( P = 0.004), lupus anticoagulant ( P = 0.013), positive IgM-aCL ( P = 0.039), positive ANA ( P = 0.002) and anti-dsDNA ( P = 0.046). The diagnostic value of hypocomplementemia in patients with SLE is based on the association with the disease activity, immune-complex mediated manifestations (glomerulonephritis, cryoglobulinemia) and APS-related features (livedo reticularis, hemolytic anemia and aPL). Hypocomplementemia was found in nearly half of patients with primary APS and was associated with some APS features (livedo reticularis, thrombocytopenia, and aPL) along with SLE-related immunological markers (ANA and anti-dsDNA), identifying a subset of patients with primary APS with a higher risk of evolving to SLE. These results clearly support the routine determination of complement factors in the clinical follow-up of patients with SLE and primary APS. [7]

In a study of 71 patients by Fofi et al. in January-February 2001, it was found that there was no association between the presence of aCL and the different WHO classes. The presence of these antibodies does not seem to be related to the histological activity or the chronicity of lupus nephritis nor proteinuria. [8] In a study of PAPS and SLE, Loizou et al. observed that raised levels of aCL are associated with lupus nephritis. In SLE they demonstrated that the presence of aCL antibodies in conjunction with elevated levels of anti-dsDNA and anti-C1q antibodies is highly specific for glomerulonephritis in patients with lupus. [9]

The significant finding is in the greater incidence of both interstitial fibrosis and tubular atrophy in aCL+ patients ( P = 0.019 and 0.052, respectively). This was in good agreement the findings of Nochy et al. , as mentioned earlier, that the histomorphological heterogeneity is attributed to APSN. At present, hyaline thrombi have been described in patients with active and usually proliferative lupus nephritis. The prevalence and significance of this finding was studied by Kant et al. [10] and Gueck et al. [11] They found the overall rate of capillary thrombosis to be approximately 50% in cases of proliferative lupus nephritis, including 78% in patients with detectable LA and only 38% in those without detectable LA. The presence of glomerular thrombi in the initial biopsy was a strong predictor of glomerular sclerosis. However, other studies have not shown an association between the antiphospholipid antibodies (aPL) and the prognosis in lupus nephritis. In a study of 111 patients with SLE for a 5-year follow-up on the basis of the aCL levels, Moroni et al. concluded that the detection of the aPL antibodies in patients with lupus nephritis is useful not only to identify patients at risk for vascular and obstetric manifestations but also for their potential deleterious impact on the renal outcomes. [12]

The study into the incidence of APSN revealed its presence in four out of 28 (14.2%) aCL+ patients ( P = 0.4). It is noteworthy that certain acute features of APSN, such as mesangial proliferation, and chronic features such as segmental and global glomerulosclerosis may be observed per se in lupus nephritis; these features can cloud the interpretation.

As is evident from the abovementioned facts, only patient 3 satisfied the classification criteria of primary antiphospholipid syndrome. Patient 3 was definite for APS as per the Alarcon-Segovia criteria and the remaining three patients with APSN were probable for the same.

The most significant histology was observed in a patient 1, who had class IV lupus with an activity of 9 and chronicity of 0 with a double contour appearance of the capillary walls and fluffy appearance of the glomerular margins. One glomerulus contained fibrinous material in its lumen. However, the blood vessels were normal. This patient improved to class IIb with the complete disappearance of the features of APSN. Capillary wall thickening was detected in all the four samples. In a retrospective study of 114 patients with lupus nephritis, Daugas et al. detected the following: (1) APSN occurs in SLE (32% of patients with renal biopsies) additionally and independently of lupus nephritis; (2) APSN is statistically associated with lupus anticoagulant, but not with aCL; (3) APSN is associated with extra renal APS, mainly arterial thromboses and obstetrical fetal loss (observed in patient 3 of our series), but not with venous thrombosis of APS; and (4) APSN is an independent risk factor over and above lupus nephritis, which contributes to an elevated prevalence of hypertension, elevated serum creatinine and increased interstitial fibrosis. Thus, it is likely that, APSN may worsen the prognosis in these patients because of its associations with hypertension, azotemia and interstitial fibrosis. APSN may also have therapeutic significance in that its recognition should permit a better balance between the immunosuppressor and the antithrombotic and/or vasoprotective therapy. Finally, this study suggests that APSN should be included in the classification criteria of APS. [13] Although our study detected APSN in only 8.3% of total renal biopsies (all in 14.2% of aCL+), it was associated with both class IIb and class IV lupus, the lesions subsequently disappeared on repeat biopsy. Hence, it was an independent finding in our study, which would assume significance when a large number of biopsies are studied. Moreover, in patients with APSN, no other thrombotic manifestations were detected in our study. In a study of 267 renal biopsies, Ferluga et al. suggested that the additional mechanisms related to the occurrence of antiphospholipid antibodies and ANCA contribute to the histomorphologic heterogeneity of WHO class III and IV lupus GN, particularly to the development of thrombotic, necrotizing and crescentic glomerular lesions. [14] Komiya et al. reported two cases of SLE with APSN. Their biopsied renal specimens showed the characteristic findings for APSN, such as mesangial proliferation, double contours, thickening of the capillary loops and intimal hyperplasia; however, there was no evidence for the immune complexes in the glomeruli, which were examined by indirect immunofluorescence and electron microscopy. These results indicated that their renal dysfunction was caused by APSN. Their experience suggested that the anticoagulant therapy in addition to corticosteroids offers advantages in the treatment of patients with SLE accompanied with APSN and renal dysfunction. [15] In a study of 151 renal lupus, Tektonidou et al. concluded that among patients with SLE, APS nephropathy occurs almost exclusively in those with aPL, suggesting an important role of aPL in the pathogenesis of APS nephropathy. Patients with APS nephropathy develop hypertension, raised serum creatinine levels and progression of histologic lesions, all of which are associated with a poor renal outcome. The manifestations of APS also tend to develop in these patients. APS nephropathy should be included in the APS classification criteria and the use of appropriate anticoagulant therapy should be tested. [16]

Among the four patients with APSN, two had aCL IgG value >5 SD from the standard population and one had a value of 2-5SD. For IgM, two patients had a value >5 SD and the remaining had values between 2 and 5 SD.

  Conclusion Top

We conclude that aCL positivity does not lead to a higher histological morbidity in lupus nephritis in terms of WHO class, activity or chronicity indices. Although there is no difference in the level of azotemia, the response in terms of hypocomplementemia is slower in aCL positive patients, especially for those into 6 months of therapy. Proteinuria did not correlate as significantly with the trends of hypocomplementemia. Antiphospholipid nephropathy, is an independent entity in lupus nephritis. Although a larger series is required to confirm our finding, this study shows that it only contributes to greater heterogeneity in lupus nephritis with no effect on renal morbidity. However, aCL positivity does contribute to greater incidence of interstitial fibrosis, tubular atrophy and capillary wall thickening in biopsy specimens. The acute lesions of APSN possibly tend to resolve in response to the therapy.

  Acknowledgements Top

We acknowledge the cooperation from Dr. Chitra Madiwale; Prof. in Pathology, Seth G.S Medical College and KEM Hospital, Parel, Mumbai.

  References Top

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2.Alarcon-Segovia D, Perez-Vasquez ME, Villa AR, Drenkard C, Cabiedes J. Preliminary classification criteria for the antiphospholipid syndrome within systemic lupus erythematosus. Semin Arthritis Rheum 1992;21:275-86.  Back to cited text no. 2    
3.Khamashta MA. Hughes Syndrome: Antiphospholipid Syndrome. Springer-Verlag London Ltd; London: 2000.  Back to cited text no. 3    
4.Fofi C, Cuadrado MJ, Godfrey T, Abbs I, Khamashta MA, Hughes GR. Lack of association between antiphospholipid antibody and WHO classification in lupus nephritis. Clin Exp Rheumatol 2001;19:75-7.  Back to cited text no. 4  [PUBMED]  
5.Naiker IP, Rughubar KN, Duursma J, Pudifin DJ, Seedat YK. Anticardiolipin antibodies in South African patients with lupus nephritis: A clinical and renal pathological study. Am J Nephrol 2000;20:351-7.  Back to cited text no. 5  [PUBMED]  [FULLTEXT]
6.Horbach DA, van Oort E, Donders RC, Derksen RH, de Groot PG. Lupus anticoagulant is the strongest risk factor for both venous and arterial thrombosis in patients with systemic lupus erythematosus: Comparison between different assays for the detection of antiphospholipid antibodies. Thromb Haemost 1996;76:916-24.  Back to cited text no. 6  [PUBMED]  
7.Ramos-Casals M, Campoamor MT, Chamorro A, Salvador G, Segura S, Botero JC, et al . Hypocomplementemia in systemic lupus erythematosus and primary anti-phospholipid syndrome: Prevalence and clinical significance in 667 patients. Lupus 2004;13:777-83.  Back to cited text no. 7  [PUBMED]  [FULLTEXT]
8.Fofi C, Cuadrado MJ, Godfrey T, Abbs I, Khamashta MA, Hughes GR. Lack of association between antiphospholipid antibody and WHO classification in lupus nephritis. Clin Exp Rheumatol 2001;19:75-7.  Back to cited text no. 8  [PUBMED]  
9.Loziou S, Samarkos M, Norsworthy PJ, Cazabon JK, Walport MJ, Davies KA. Significance of anticardiolipin and anti-beta(2)-glycoprotein I antibodies in lupus nephritis. Rheumatology (Oxford) 2000;39:962-8.  Back to cited text no. 9    
10.Kant KS, Pollack VE, Weiss MA, Glueck HI, Miller AN, Hess EV. Glomerular thrombosis in SLE: Prevalence and significance. Medicine (Baltimore) 1981;60:71-86.  Back to cited text no. 10    
11.Gueck HI, Kant KS, Weiss MA, Pollak VE, Miller MA, Coots M. Thrombosis in SLE: Relation to the presence of circulating anticoagulants. Arch Intern Med 1985;145:1389-95.  Back to cited text no. 11    
12.Moroni G, Ventura D, Riva P, Panzeri P, Quaglini S, Banfi G, et al . Antiphospholipid antibodies are associated with an increased risk for chronic renal insufficiency in patients with lupus nephritis. Am J Kidney Dis 2004;43:28-36.  Back to cited text no. 12  [PUBMED]  [FULLTEXT]
13.Daugas E, Nochy D, Huong DL, Duhaut P, Beaufils H, Caudwell V, et al . Antiphospholipid syndrome nephropathy in systemic lupus erythematosus. J Am Soc Nephrol 2002;13:42-52.  Back to cited text no. 13  [PUBMED]  [FULLTEXT]
14.Ferluga D, Jerse M, Vizjak A, Hvala A, Rozman B, Kos-Golja M, et al . Correlation among WHO classes, histomorphologic patterns of glomerulonephritis and glomerular immune deposits in SLE. Wien Klin Wochenshr 2000;112:692-701.  Back to cited text no. 14    
15.Komiya T, Okamura M, Kawakami K, Okazaki M, Tsukamoto J, Okada S, et al . Two cases of systemic lupus erythematosus accompanied by antiphospholipid syndrome nephropathy without immune complex nephritis. Nippon Jinzo Gakkai Shi 2002; 44:817-22.  Back to cited text no. 15  [PUBMED]  
16.Tektonidou MG, Sotsiou F, Nakopoulou L, Vlachoyiannopoulos PG, Moutsopoulos HM. Antiphospholipid syndrome nephropathy in patients with systemic lupus erythematosus and antiphospholipid antibodies: Prevalence, clinical associations, and long-term outcome. Arthritis Rheum 2004;50:2569-79.  Back to cited text no. 16  [PUBMED]  [FULLTEXT]


  [Figure - 1], [Figure - 2], [Figure - 3], [Figure - 4], [Figure - 5], [Figure - 6], [Figure - 7], [Figure - 8]

  [Table - 1], [Table - 2], [Table - 3], [Table - 4], [Table - 5], [Table - 6]

This article has been cited by
1 Renal involvement in antiphospholipid syndrome
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[Pubmed] | [DOI]


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