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Table of Contents
ORIGINAL ARTICLE
Year : 2014  |  Volume : 2  |  Issue : 1  |  Page : 12-19

Clinicopathological characteristics of lupus nephritis in Western region of Saudi Arabia: An experience from two tertiary medical centres


1 Department of Pathology, Faculty of Medicine, King Abdulaziz University, Jeddah, Saudi Arabia; Department of Pathology, Faculty of Medicine, Minia University, El Minia, Egypt
2 Department of Medicine, Faculty of Medicine, King Abdulaziz University, Jeddah, Saudi Arabia
3 Department of Medicine, King Faisal Specialist Hospital and Research Centre, Jeddah, Saudi Arabia
4 Department of Pathology, Faculty of Medicine, King Abdulaziz University, Jeddah, Saudi Arabia

Date of Web Publication29-Jan-2018

Correspondence Address:
Wafaey Gomaa
Department of Pathology, Faculty of Medicine, King Abdulaziz University, P.O. Box: 80205, Jeddah 21589, Saudi Arabia

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Source of Support: None, Conflict of Interest: None


DOI: 10.1016/j.jmau.2014.02.001

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  Abstract 


Background: We present the clinicopathological characteristics of lupus nephritis (LN) in a subset of population from Western Saudi Arabia.
Materials and methods: We retrospectively analysed previously diagnosed 148 renal biopsies in cases with systemic lupus erythematosus (SLE) from two medical centres. Microscopic slides from these patients were retrieved and re-assessed according to the WHO and ISN/RPS classifications by histological, immunological and electron microscopic items. Clinical and laboratory findings were retrieved from patient's medical records.
Results: Median age of patients years is 24 (range: 2–65), females (85.1%), and males (14.9%). The frequency of cases in each class according to WHO classification and ISN/RPS classification was nearly the same and was as follows: class I (0%), class II (12.8%), class III (8.8%), class IV (51.4%), class V (23%), and class VI (4%). For IV class, IV-G (41.9%) subcategory was higher than IV-S (9.4%). Immunofluorescence examination revealed positive staining for IgG and C3 in 98.4% and 97.6% of cases respectively. In conclusion, class IV (51.4%) is the predominant class, followed by class V (23%).
Conclusion: There are differences in clinicopathological data reported from this study with other studies. Continuous reporting from different national specialised nephrology centres is recommended for better elucidation of the natural history of lupus nephritis in Saudi patients.

Keywords: Lupus nephritis, Histopathology, Clinical, Laboratory, Saudi Arabia


How to cite this article:
Gomaa W, Bahlas S, Habhab W, Mushtaq M, Al-Ghamdi S, Al-Maghrabi J. Clinicopathological characteristics of lupus nephritis in Western region of Saudi Arabia: An experience from two tertiary medical centres. J Microsc Ultrastruct 2014;2:12-9

How to cite this URL:
Gomaa W, Bahlas S, Habhab W, Mushtaq M, Al-Ghamdi S, Al-Maghrabi J. Clinicopathological characteristics of lupus nephritis in Western region of Saudi Arabia: An experience from two tertiary medical centres. J Microsc Ultrastruct [serial online] 2014 [cited 2022 Sep 29];2:12-9. Available from: https://www.jmau.org/text.asp?2014/2/1/12/224203




  1. Introduction Top


Systemic lupus erythematosus (SLE) is a chronic disease with autoimmune pathogenesis and manifests as low grade inflammation and may advance to multiorgan fatal damage [1]. In SLE patients who have abnormal urine and/or reduced renal function, renal biopsy is performed to provide prognostic data and direct the initial therapeutic approach [2]. The incidence of lupus nephritis (LN) in SLE is divergent around the world and may be related to different ethnic and genetic background [3],[4],[5].

Most patients with LN have an immune complex-mediated glomerular disease, often associated with tubulointerstitial changes with or without immune deposits. Involvement of the renal vasculature is also common, ranging from indolent vascular immune deposits to fibrinoid necrosis and thrombotic microangiopathy [6]. Renal involvement is reflected by different clinical and laboratory manifestations which vary considerably around different geographic distribution [5].

Currently, renal histological changes are identified according the International Society of Nephrology (ISN)/Renal Pathology Society (RPS) Classification of LN [7] which is entirely based on glomerular changes. It was designed to eliminate ambiguities and standardise definitions. Major changes from 1995 modified WHO classification [8] include better standardisation of renal biopsies in lupus patients [7] and separation of segmental and global lesions [9] which was suggested by a study in 2000 [10] who concluded that cases with diffuse proliferative LN and segmental lesions have poorer prognosis than those with global diffuse proliferative.

We aim in this study to evaluate the pathological and clinical characteristics of a subset of LN cases from two medical centres in the Western region of Saudi Arabia and compare these findings with findings from other regions in Saudi Arabia, near-by countries, and international figures.


  2. Materials and methods Top


The study group comprised a total of 148 biopsies diagnosed as lupus nephritis from two large tertiary medical centres in Jeddah (Western region of Saudi Arabia); King Abdulaziz University Hospital (period from 1995 to 2011) and King Faisal Specialist Hospital and Research Centre (2000–2011). Patient’s histological materials were retrieved from the archive of department of Pathology in the above mentioned centres. The microscopic criteria described in LN, and the definition ofterms, were collected from the literature. The renal biopsy specimens were studied by light microscopy, immunofluorescence, and electron microscopy. Haematoxylin and Eosin (H&E), Periodic Acid-Schiff (PAS), Masson Trichrome and Jones Methenamine Sliver (JMS) stained slides of cases were re-examined to retrieve data according the standards of defining diagnostic terms reported elsewhere [11].

The activity and chronicity indices (AI and CI) were retrieved if were reported whenever possible and re-reported for cases that were not reported using the semi-quantitative scoring schema developed by Austin et al. [12]. Each activity and chronicity factor is graded on a scale of 0, 1, 2, and 3 depending on the percentage of involvement of all viable glomeruli (AI) and on all glomeruli (CI) present in sections; where 0 (absence of lesions), 1 (lesions involving up to 25%), 2 (lesions involving 25–50%), and 3 (lesions involving >50%). The activity items cellular crescents and necrosis are weighed by a factor of x2.

Results of immunofluorescence for immunoglobulin G (IgG), immunoglobulin A (IgA), immunoglobulin M (IgM), C3, C4, C1q and fibrinogen deposits were semi-quantitatively graded from 0 to 4 according to the intensity of fluorescence. The immunofluorescence findings of each patient were collected and analysed. Electron microscopy reports were used whenever needed for subendothelial, subepithelial, mesangial and intramembranous electron dense deposits. Renal involvement was assessed and cases were reclassified using both the modified WHO and ISN/RPS classifications {wherever were not used}. For categorisation of classes III and IV of ISN/RPS classification, active lesions were considered according to the presence of cellular crescents, fibrinoid necrosis, and a chronic lesion when glomerular sclerosis, and interstitial fibrosis are present [7].

Patients’ clinical data were collected from the medical archives of departments of Internal medicine. The clinical findings were analysed as patient’s age, sex, nationality, the presence of hypertension, diabetes, renal dialysis before and after renal biopsy, renal impairment before renal biopsy, and nephrotic syndrome. Laboratory results were also analysed including; haemoglobin, erythrocyte sedimentation rate ESR, serum C3, C4, antinuclear antibodies (ANA), anti-DNA, CRP, anti-cardiolipin IgM, anti-cardiolipin IgG, urine protein, urine RBC, Urine cast, and 24 h protein were also retrieved. Revision of therapies applied were also collected; hydroxychloroquine (Plaquenil®) azathioprine, cyclophosphamide, pulse steroid prednisone, mycophenolate mofetil (CellCept®), methotrexate, cyclosporine. Patient mortality records were collected.

The work in this study was in accordance with the ethics committee of Faculty of Medicine, King Abdulaziz University, Saudi Arabia, and according to the ethical guidelines of the 1975 Declaration of Helsinki. Statistical analysis was done in the Statistical Package for Social Sciences (SPSS®) version 16. Frequencies and results were presented as median (range).


  3. Results Top


Median age of patients is 24 years and range is (2–65). Females constitute 126 (85.1%) and males 22 (14.9%) with female to male ratio 5:1. In the patient's population, 97 (65.5%) of them were Saudi and 51 (34.5%) were non-Saudi.

3.1. Pathological features

The mean and standard deviation (SD) of activity and chronicity indices are 7.2454 (4.6993) and 3.0629 (2.3088) respectively. In a range between 15.5% and 83.1% of cases immunofluorescence results could not be reported in this study. Reasons are; no tissue available, sclerosed glomeruli, missing surgical pathology report, not done, no glomeruli in sections, or patients presented to these centres with paraffin embedded blocks for referral. IgG and IgA showed positivity in 98.4% and 82% of cases respectively. IgM showed positivity in 90.3%. C3 and C4 showed positivity in 97.6% and 49.3% respectively. C1q was positive in 88% of cases. Fibrinogen was positive in 32% of cases done [Table 1].
Table 1: Distribution of immunofluorescence findings.

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The frequency of cases in each class within the WHO classification and ISN/RPS classification is shown in [Table 4], [Table 5]. The frequency of each class is as follows: none of cases classified as class I. Within WHO classification; class II (12.8%), class III (8.8%), class IV (51.4%), class V (23%), and class VI (4%). While within ISN/RPS classification; class II (12.85%), class III (8.8%), class IV (51.3%), class V (22.9%), and class VI (4%). Subcategories falling in class III in both classifications were the same. For class IV in WHO classification [Table 2], active lesions (IV-B) were the highest among other subclasses (27.7%) while segmental lesions were the lowest (6.1%). In class IV within ISN/RPS [Table 5], global lesions were higher (41.9%) than segmental lesions (9.4%). In segmental lesions; there is no difference between subcategories {IV-S (A), (C) and (A/C)}, while in global lesions the active and chronic lesions were the highest (22.3%) among other subcategories. [Figure 1],[Figure 2],[Figure 3] represent histological, immunofluorescence, and electron microscope findings in selected cases.
Table 4: Distribution of clinical findings.

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Table 5: Distribution of laboratory findings.

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Table 2: Distribution of cases falling in each class in modified WHO classification (1995).

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Figure :1 (A) Lupus class II (mesangial proliferative lupus nephritis). A glomerulus shows mild mesangial hypercellularity (H&E) 200×. (B) Lupus class III (focal lupus nephritis). Aglomerulus shows segmental endocapillary hypercellularity, mesangial hypercellularity, and capillary wall thickening (JMS) 200×. (C) and (D) Lupus class IV (diffuse lupus nephritis) G–AC. Global severe endo- and extracapillary proliferation, wireloop lesions, leucocyte influx and mesangial expansion with hypercellularity (C stained with H&E) and (D stained with JMS) 200×.

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Figure 2: (A)and(B) Lupus class IV S-A. A glomerulus shows diffuse segmental proliferative and sclerosing lupus nephritis (A stained with H&E) and (B stained with JMS) 200×. (C) Lupus class V (membranous lupus nephritis). Global subepithelial and subepithelial spike formation (JMS) 200×. (D) Lupus class VI (advanced sclerotic lupus nephritis). A glomerulus with diffuse, global glomerular sclerosis with interstitial mononuclear inflammatory infiltrates (H&E) 200×.

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Figure 3: (A) Immunofluorescence for IgG shows positive staining in a case of lupus nephritis (arrow). (B) Immunofluorescence for c3 shows positive staining in a case of lupus nephritis (arrow). (C) Electron micrograph of lupus nephritis reveals numerous discrete electron dense “immune-type” deposits mainly in mesangial area with some in subepithelial and subendothelial areas (arrow). (D) Electron micrograph of another case of lupus nephritis showing mainly intramembranous electron dense deposits (arrow).

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3.2. Clinical findings

Out of 148 cases retrieved, a range of5.4-48.65% of cases there were partially missing clinical and laboratory data [Table 3]. The range of duration of lupus nephritis is 6–408 months while the median is 84 months. In this study, 8 (6.1%) of patients were diabetic, 88 (62.9%) patients were hypertensive, 76 (58.5%) patients had nephrotic syndrome, and 47 (34.8%) had renal impairment prior to renal biopsy. Patients were subjected to renal dialysis for impaired renal function in 6.1% of cases before taking renal biopsy. While in 18.7% of cases renal dialysis was performed after renal biopsy. Mortality rate represent 3.2% of the study group. The cause of death was not reported. Data is shown in [Table 4].
Table 3: Distribution of cases falling in each class in ISN/RPS classification (2003).

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3.3. Laboratory findings

[Table 5] shows all the laboratory abnormalities in our patients. Anti-nuclear antibody and anti-DNA antibody were positive in 95.7% of tested patients. Elevated ESR and CRP were found in 77 (82.8%) and 59 (74.7%) of tested patients respectively. Complements C3 and C4 were low in 91 (80.5%) and 98 (86.7%) of tested patients respectively. Anti-cardiolipins IgM and IgG showed elevated levels in 13.2% and 26.3% of tested cases respectively. Proteinuria and urinary cast was reported in 75 (77.3%) and in 58 (63%) of patients. While 24 h protein showed positivity in 105 (89.7%) tested cases. Haematuria was reported in 101 (88.6%) patients.

3.4. Treatments

Frequency of drugs administered is shown in [Table 6]. 73.3% of patients were treated with Plaquenil®. CellCept® was the second most frequently administered drug. Azathioprine and cyclophosphamide were administered in equal percentage of patients.
Table 6: Frequencies of therapeutics used.

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  4. Discussion Top


There is a large literature regarding the clinicopathological criteria ofLN. However, these findings are still reported with discrepancies from different regions of the world. King Abdulaziz University and King Faisal Specialised Hospitals are two large tertiary medical centres in Western region of Saudi Arabia and are referral centres for LN. This study represents a large series of LN reported from Saudi Arabia. Currently, there are no uniform national figures about data on LN from Saudi Arabia. Previously, the incidence of LN in SLE patients in Saudi Arabia had been reported from different areas different occasions. In Riyadh region was 63% in 1995 [13], 53.7% in 2007 [14], and 47.9% in 2009 [15]. In Western region was 55.4% [16], and 61% [17]. The present study represent a cohort study from a subset of LN patients in Western Saudi Arabia attempting to provide data on the prevalence, clinicopathological features, and therapy of LN patients and compare them to other studies both regionally and internationally.

In this study, the median age and age range together with sex predilection from this subset of cases are comparable with many international and national reports about LN [16],[18],[19]. However, the median age is lower than reported by a study from central Asia [20], and also lower than a large study from the Eastern region of Saudi Arabia [15]. Also, the female: male ratio was higher than previously reported [15]. The reason of difference may be referred to difference ethnic distribution; as in our study the Saudi population represents 65.5% patients while in their study this was 88.6%.

Although eclipse of 8 years since the introduction of ISN/RPS classification, we found that in these two centres this classification is less frequently used and instead there is a heterogeneous mix of WHO classifications (1982 and 1995) and sometimes ISN/RPS classification were used. In this study, we re-classified this subset of cases according to both currently used classifications. The findings regarding the distribution of classes are similar to reports from different region continents. We found that diffuse proliferative LN (class IV) is the most frequent pathological lesion in our subset of cases. This finding is similar to previous reports [5],[15],[18],[19],[21],[22],[23],[24],[25]. However, some studies from Arab countries showed higher incidence within class III [26],[27], this difference from our finding is probably related to small sample size used in these studies or different ethnic groups. Global lesions of class IV in the ISN/RPS 2003 classification were higher than segmental lesions which is similar to findings of others [19],[28]. Also the active and chronic lesions were the highest (23.9%) among other subcategories of IV-G which in concordance of Yokoyama et al. [19]. Results for activity and chronicity indices are higher than those reported by Hiramatsu et al. [29], the cause is that we used a larger sampler. In the meantime, other studies were similar to ours [30] as this study used a larger sample. In the ISN/RPS 2003 classification of LN the description of classes III and IV depends on the reporting of activity and chronicity which depends on the proportion of glomeruli with active and chronic lesions.

In our study, we found a considerable number of cases lacking the reporting of activity and chronicity features in original pathology reports and in cases that reported pathologists were inconsistent. Some mentioned the final numerical sum, in few cases the detailed items were mentioned in microscopic description and final diagnosis. The microscopic description of each item of scoring is important to be reported because some active features (subendothelial deposits or interstitial inflammation) are therapeutically reversible while others like cellular crescents or necrosis are not [31]. IgG immunofluorescence is predominant among immunoglobulins which are associated with early complements C1q, C4 as well as C3 similar to other reports [32].

In our study, patients presenting with hypertension constitutes 62.9%, which is higher than reported from previously reported [15],[25],[30]. A small percentage of patients were diabetic which may be related to steroid treatment. Our results for ANA is similar to reported from other national and regional studies [5],[15]. While these results are higher than reported from a study from East Asia (78.4%) [20]. This is referred to our large series of cases. The anti-DNA is higher than the range reported before [5],[15],[20]. Anti-cardiolipins were found elevated in a small percentage (13.2% and 26.3%) which is far lower than the range reported by Jallouli et al. [5] (71.6%) but comparable to other studies [27],[33]. Levels of complements (C3 and C4) were low in 80.5% and 86.8% of tested patients. These figures are higher than other studies [5],[15]. In a national study, C3 was observed in low levels in half of cases which was associated with poor survival [15]. Proteinuria was found in 77.3% of cases which is higher than reported in other studies [15],[18],[24]. The mortality in this study is low and is similar to previous finding from Western Saudi Arabia [16] and lower than from Eastern Saudi Arabia [15]. The improved survival rate in LN is attributed to early diagnosis, improved patients response to treatment modalities.

The limitations of our study were unavailability of a portion of clinical and pathological data including full survival data, and lack of treatment outcome history.


  5. Conclusion Top


We have presented a series of LN in Western Saudi Arabia and compared with results from other series. Class IV was the most frequent type of nephritis seen in our patients. The usage of ISN/RPS in these two centres is still limited. We do encourage pathologists to use the activity and chronicity indices in details and to use ISN/RPS classification. There is still some discrepancies regarding clinicolaboratory features of LN among national and regional areas. Continuous reporting from different national specialised nephrology centres is recommended for awareness of the magnitude of this disease in Saudi Arabia.

Conflict of interest

The authors declare that there are no conflicts of interest.



 
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    Figures

  [Figure 1], [Figure 2], [Figure 3]
 
 
    Tables

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


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