|Ahead of print publication
Spectrum of renal histopathologic lesions in patients with nonlupus rheumatologic diseases
Pallavi Prasad, Mithlesh Bhargav, Alka Singh, Vinita Agrawal, Manoj Jain
Department of Pathology, SGPGIMS, Lucknow, Uttar Pradesh, India
|Date of Submission||06-May-2022|
|Date of Acceptance||29-Jun-2022|
|Date of Web Publication||18-Aug-2022|
Room No. 11, C-Block, Department of Pathology, SGPGIMS, Lucknow, Uttar Pradesh
Source of Support: None, Conflict of Interest: None
Background: Nonlupus rheumatic diseases regularly involve solid organs, including the kidney. Renal lesions can be either a manifestation of the same systemic disease, a side effect of drug therapy, or an unrelated renal disease. Our aim was to evaluate the spectrum of renal histopathological lesions found in this group of patients.
Methods: Native renal biopsies of patients with systemic rheumatic disorders received between January 2014 and August 2019 were reviewed, along with their immunofluorescence findings. The clinical data were recorded from the Hospital Information System. Patients with systemic lupus erythematosus were excluded.
Results: Eighty-one clinically diagnosed cases of nonlupus rheumatic diseases were studied (age range 8–70 years, mean 42.8 years, male: female ratio 1:1.3). The most common systemic autoimmune disease was anti-neutrophil cytoplasmic antibodies -associated vasculitis (n = 21) followed by immunoglobulin-A (IgA) vasculitis (Henoch-schonlein purpura) (n = 12) and rheumatoid arthritis (n = 10). The most common histopathological lesion was pauci-immune crescentic glomerulonephritis (n = 26), followed by IgA nephropathy (n = 12) and amyloidosis (n = 8). All patients were treated as per the standard therapeutic regimens.
Conclusion: A diverse group of renal lesions can be found in patients with rheumatic disorders. The diagnosis of such lesions aids the clinician in the decision-making for either intensifying or reducing the drug therapy and in predicting the prognosis.
Keywords: Histopathology, pauci-immune, renal lesions, rheumatic diseases, vasculitis
| Introduction|| |
Rheumatic diseases are systemic autoimmune diseases that mainly affect the joints and soft tissues and can sometimes affect solid organs such as the kidneys. A lower glomerular filtration rate was found in patients with rheumatic diseases compared to the general population. Renal involvement in rheumatic diseases is exacerbated by several other factors such as diabetes, hypertension, cardiovascular complications, chronic inflammation, and long-term use of nephrotoxic agents. The renal disease may be a manifestation of the systemic rheumatic disease or a result of the drug-therapy. At times, it may be totally unrelated to the rheumatic disease.
A large body of the literature is available on lupus nephritis, and many studies have reported the predominant clinical and pathophysiological features of renal involvement in individual rheumatic diseases. The present study aims to evaluate the spectrum of renal histopathologic lesions resulting from primary rheumatic diseases other than systemic lupus erythematosus (SLE).
| Methods|| |
In this retrospective study, native renal biopsies in patients with clinically diagnosed rheumatologic diseases which were received in the Department of Pathology between January 2014 and August 2019 were reviewed by an experienced nephropathologist. The indications of the renal biopsy were raised serum creatinine levels, hematuria, proteinuria, or a combination of these. The clinical and laboratory data were recorded from the Hospital Information System. Of the total 2977 renal biopsies received, patients with SLE were excluded from the study and 81 patients with nonlupus known rheumatologic disease were included in the study.
Renal biopsy processing
Biopsy tissue for light microscopy was fixed in 10% formalin, embedded in paraffin, sectioned (23 μm) and stained with hematoxylin and eosin, periodic acid Schiff, Masson's trichrome and methenamine silver. For immunofluorescence, tissue was placed in a compound with optimal cutting temperature and snap-frozen in liquid nitrogen. Fluorescein isothiocyanate-conjugated primary anti-human rabbit polyclonal antibodies against immunoglobulins (Ig)-IgG, IgA, IgM, C1q, C3, and light chains were used. The intensity of staining was rated semi-quantitatively on a scale of 0–3+ (1+, weak staining; 2+, moderate staining; 3+, strong staining). Electron microscopy was performed on eleven biopsies. For electron microscopy, tissue was fixed in 3% buffered glutaraldehyde (pH 7.4) and postfixed in osmium tetroxide. After routine processing and embedding in epoxy, thin sections were cut and stained with uranyl acetate and lead citrate. The ultrastructural examination was performed using a transmission electron microscope (Jeol 1400+).
Routine and immunological workup
Complete urine (routine, spot, and 24-h urinary protein) and hematological parameters (hemoglobin, total leukocyte count, platelet count, and erythrocyte sedimentation rate [ESR]) were available in all cases. Relevant serological workup including creatinine, serum complements C3 and C4, acute-phase reactants, autoantibodies (anti-nuclear antibody (ANA), anti-double-stranded DNA (Anti-ds DNA), anti–Sjogren's-syndrome-related antigen A autoantibody (Anti-SSA/Ro antibodies), anti-Sjogren's syndrome Type B antibody (Anti-La/SS-B antibodies), anti-cyclic citrullinated peptide antibody, anti-proteinase 3 (PR 3) anti-neutrophil cytoplasmic antibody, anti-myeloperoxidase (MPO), anti-glomerular basement membrane (anti-GBM) antibody, and antiphospholipid antibodies were done as and when indicated.
| Results|| |
A total of 2977 native kidney biopsy specimens were received during the 6-year study period. Out of these, 81 patients who had a history of systemic autoimmune diseases, presented with renal dysfunction and underwent a native kidney biopsy were studied. The patients were aged 8–70 years, with a mean of ~42.8 years. Thirty five patients (42%) were male and 47 (58%) were females (male: female ratio of 1:1.3). Demographics and laboratory data are summarized in [Table 1]. Comorbid conditions such as hypertension and diabetes were found in 22.2% (n = 18) of study subjects. Laboratory investigations revealed proteinuria, hematuria, and a rise in serum creatinine, either isolated or in combination.
The most common systemic autoimmune disease was anti-neutrophil cytoplasmic antibodies (ANCA)-associated vasculitis (AAV) (n = 21) followed by IgA vasculitis (Henoch-schonlein purpura [HSP]) (n = 12) and rheumatoid arthritis (RA) (n = 10). The spectrum of all rheumatic diseases encountered in our study is depicted in [Table 2]. The most common histopathological lesion was pauci-immune crescentic glomerulonephritis (n = 26), followed by IgA nephropathy (n = 12) and amyloidosis (n = 8). The histological lesions encountered in various rheumatic diseases are enumerated in [Table 3] and [Figure 1] and [Figure 2]. Two cases with a known history of gouty arthritis and ankylosing spondylitis (AS) were found to have diabetic nephropathy on renal biopsies in the form of mesangial expansion and hyalinosis [Figure 2]d.
|Figure 1: (a) Pauci-immune crescentic GN in a case of GPA (PAS, ×100). (b) Partial fibrocellular crescents in a case of anti-GBM disease (PAS, ×100) (c) Glomeruli showing mesangial proliferation in a case of HSP (PAS, ×200). (d) Segmental sclerosis in a case of rheumatoid arthritis (PAS, ×400) (e) diffuse capillary wall thickening in a case of psoriasis (PAS, ×100). (f) Uniform argyrophilic epimembranous spikes in case (e) (PSM, ×1000). GN: Glomerulonephritis, GPA: Granulomatosis with polyangiitis, HSP: Henoch-schonlein purpura, PAS: Periodic acid schiff, PSM: Periodic acid silver methenamine|
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|Figure 2: (a) Case of Sjogren's syndrome showing chronic tubulointerstitial nephritis (PAS, ×100). (b) Interstitial granuloma in a case of sarcoidosis (H and E, ×100). (c) Hypertensive vasculopathy in scleroderma renal crisis (H and E, ×100). (d) Hyalinosis in a case of diabetic nephropathy (PAS, ×400). (e). Case of ankylosing spondylitis displaying amyloid deposits (H and E, ×400), deposits showing apple-green birefringence on polarising microscopy (inset). (f) Randomly arranged non-branching amyloid fibrils (TEM). H and E: Hematoxylin and eosin, PAS: Periodic acid schiff, PSM: Periodic acid silver methenamine, TEM: Transmission electron microscopy|
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|Table 2: Spectrum of rheumatic diseases, indications of renal biopsy, and respective renal histologic lesions (n=81)|
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|Table 3: Distribution of renal histological lesions in rheumatic diseases|
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Autoimmune parameters, serology, immunofluorescence, and electron microscopic findings were supportive in all the cases. Immunohistochemistry for anti-phospholipase A2 receptor antibody was negative in all the three cases of membranous nephropathy. The patients were treated as per the standard therapeutic regimens.
| Discussion|| |
Systemic autoimmune diseases are caused as a result of the dysregulated immune system, in which the immune cells of the body attack the autoantigens and cause tissue injury. These include diseases such as RA, SLE, systemic sclerosis, SS, psoriatic arthritis, vasculitis, and mixed connective tissue disorders. Involvement of vital organs (lung and kidney) invariably occurs as the disease progresses and is a major cause of mortality.
The renal involvement in rheumatic diseases may have varied clinical manifestations depending on the severity and duration of the disease and the part of the nephron damaged. For instance, patients with RA may have renal amyloidosis, which is characterized by the deposition of amyloid fibrils mainly in glomeruli, blood vessels, or tubulointerstitium. The glomeruli are the most common site of renal involvement in SLE. Primary pSS is characterised by tubulointerstitial nephritis (TIN), whereas rapid progressive glomerulonephritis (RPGN) is the most common presentation in ANCA-associated small-vessel vasculitis.
Rapidly progressive renal failure (RPRF) is marked by a rapid decline in renal function along with nephritic urine sediment and a normal or enlarged kidney. The causes of RPRF include anti-GBM antibody disease, pauci-immune glomerulonephritis, and immune-complex mediated glomerulonephritis. The diagnosis is established by renal biopsy findings along with serological testing for C3, C4, cytoplasmic ANCA, perinuclear ANCA (c-ANCA, p-ANCA), ANA, dsDNA, cryoglobulins, and anti-GBM antibodies. Thirty cases in the present study presented with RPRF, which on further workup were diagnosed later as pauci-immune crescentic glomerulonephritis (n = 26) and anti-GBM disease (n = 4).
The Revised International Chapel Hill Consensus Conference Nomenclature of Vasculitides defines anti-GBM disease as an immune-complex, small-vessel vasculitis. It is marked by the presence of circulating and deposited antibodies directed against basement membrane antigens. The majority of the affected patients reveal the presence of injured glomeruli along with crescents in renal biopsies, which is considered a histologic hallmark of the disease. The degree of renal impairment at the time of presentation depends on the number of crescents identified in a biopsy. We encountered the four cases of anti-GBM glomerulonephritis which revealed crescentic glomerulonephritis on light microscopy, elevated serum anti-GBM antibodies, and linear IgG deposition along the glomerular capillaries on immunofluorescence microscopy. The standard treatment protocol involves the use of plasma exchange, steroids, and cytotoxic therapy to eliminate the offending autoantibodies.
Cases of pauci-immune glomerulonephritis show a lack of glomerular immunoglobulin deposits in renal biopsies. Few cases of pauci-immune crescent glomerulonephritis are idiopathic, while most patients develop pauci-immune RPGN as a manifestation of c-ANCA-or p-ANCA-associated vasculitis. In our study, we encountered 25 cases with histopathologic diagnoses of pauci-immune crescentic GN, 5 of whom progressed to diffuse global glomerulosclerosis. Etiologies were AAV, granulomatosis with polyangiitis (GPA), and eosinophilic GPA (EGPA) in 19, 5, and 1 cases, respectively. There was one case with a histopathologic diagnosis of crescent glomerulonephritis (ANCA+) occurring in the background of AS. Common renal lesions associated with AS include membranous nephropathy after etanercept therapy, IgA nephropathy, and amyloidosis. However, (ANCA)-negative pauci-immune glomerulonephritis is one of the rare autoimmune diseases associated with AS and one such case was reported by Güvercin et al., which was accompanied by pulmonary haemorrhage.
The 2012 Chapel Hill Consensus Conference Nomenclature of Vasculitides defines AAV as a necrotizing vasculitis, chiefly involving small vessels and showing sparse or no immune deposits on immunofluorescence. AAV is associated with either antibody specific for MPO-ANCA or PR3-ANCA. AAV is further classified into microscopic polyangiitis, GPA, EGPA as well as renal-limited vasculitis with pauci-immune necrotizing GN.
The second most common histopathological finding arising in the background of autoimmune diseases was observed to be IgA nephropathy. A total of 12 cases were identified and all were exclusively associated with HSP. All cases fulfilled the European League against Rheumatism and the Pediatric Rheumatology European Society criteria for (HSP/IgAV) and were classified using MEST-C light microscopy scores (mesangial hypercellularity [M], endocapillary hypercellularity [E], segmental glomerulosclerosis [S], tubular atrophy/interstitial fibrosis [T], and crescents [C]). There were significant granular IgA mesangial deposits on immunofluorescence, varying in intensity from 2+ to 4+.
The extracellular deposition of serum amyloid A protein fibrils leads to AA/secondary amyloidosis. Such amyloidosis may be secondary to any chronic inflammatory condition such as RA, AS, psoriatic arthritis, chronic infections, inflammatory bowel disease, familial periodic fever syndromes, and certain neoplasms. Two of our cases were related to RA, AS and psoriatic arthritis, while one case was observed related to sarcoidosis and SS. Rare cases with histopathological diagnosis of amyloidosis have also been observed in connection with sarcoidosis and SS, which was reported by Rajagopala et al. and Ben Abdelghani et al., In our cases, amyloidosis was the likely result of chronic inflammation resulting from the basic rheumatic disease.
TIN commonly occurs in systemic autoimmune diseases such as sarcoidosis, SS, and SLE. The mechanism involves leukocyte activation, deposition of immune complexes, complement activation, and release of inflammatory cytokines and growth factors. TIN is usually chronic in nature, although acute forms can also occur. We encountered six cases, three of which were associated with SS, while the remaining three were on a background of RA, psoriatic arthritis, and AAV, respectively. Certain drugs such as adalimumab, used in many chronic inflammatory diseases, including RA, AS, psoriatic arthritis and Crohn's disease, cause side effects such as opportunistic or granulomatous infections, nonHodgkin's lymphoma, skin lesions, heart failure, neurological demyelinating diseases, immunogenicity, induction of autoimmunity, and sarcoid-like granulomas. Justo Ávila et al. reported that granulomatous disease can induce TIN in patients treated with adalimumab. A study by Hassani et al. established that acute TIN rarely can be associated with AAV.
We also encountered three cases with a histopathologic diagnosis of granulomatous interstitial nephritis (GIN), two of whom had sarcoidosis, while a single case had RA. GIN is rare, occurring in 0.50.9% of all renal biopsies. GIN is known to be associated with the use of medications such as nonsteroidal anti-inflammatory drugs (NSAIDs) and conditions such as sarcoidosis, tuberculosis, fungal infections, and GPA. Tumor necrosis factor inhibitors used in the treatment of RA are associated with the induction of autoimmunity and the formation of sarcoid-like granulomas, which could be the possible cause of GIN in RA. A kidney biopsy is essential to establish this diagnosis, and the extent of tubular atrophy and interstitial fibrosis can help determine the prognosis.
We encountered three cases of mesangial proliferation, two associated with RA and one with GPA. Mesangial proliferation in RA has been reported previously in earlier studies also. In a large study comprising a cohort of 376 RA patients, glomerular amyloidosis followed by mesangioproliferative glomerulonephritis was the most frequent renal lesion noted. In a study done by Muthukumar P et al., mesangioproliferative glomerulonephritis was reported to be the most common histological finding in their study of 90 patients with RA (36.7%). The association of GPA with mesangioliferative glomerulonephritis is a rare occurrence, with an anecdotal case reported by Joerg et al. They concluded that the exact relation between mesangioproliferative glomerulonephritis with RA is still unclear.
Focal segmental glomerulosclerosis (FSGS) is caused by scarring following podocyte injury, resulting in increased permeability of the glomerular filtration barrier, resulting in massive proteinuria and consequent deterioration in renal function. We encountered four cases, two of which were associated with RA and one each with GPA and AAV. The main histological patterns observed in RA are amyloidosis, papillary necrosis, chronic interstitial nephritis, vasculitis, capillary proliferative glomerulonephritis and rarely, FSGS. It is believed that these renal changes are mediated by an immunological or nephrotoxic effect of specific anti-inflammatory drugs used in the treatment of RA. Similarly, an association of FSGS with AAV and GPA was observed as reported by Singh et al. and Ibrahim.,
We found three cases of membranous nephropathy accompanied by systemic autoimmune disorders such as drug-induced vasculitis, psoriatic arthritis, and mixed connective tissue disorder. Looking upon past literature, few case reports and reviews were published establishing an association of histopathological diagnosis with the above autoimmune disorders.,,
Three cases of minimal change disease (MCD) were also seen, out of which two were associated with RA, and one was associated with EGPA. Matsubara et al. concluded that MCD is associated with NSAID or d-penicillamine-induced nephropathy in RA in low incidence.
Two cases with known underlying history of gout and AS were found to have diabetic nephropathy. The most common histopathological diagnoses seen in gout are usually membranous nephropathy and amyloidosis; however, the patient was later diagnosed to be diabetic and was evaluated accordingly. A study by Mauer and Doria has shown that high serum levels of UA are a strong predictor of DN progression. Similarly, case report by Lin et al. established that HLA B27-related diseases such as AS, ulcerative colitis, and anterior uveitis syndrome can be seen in a known diabetic patient.
A total of five cases with histopathological diagnoses of hypertensive vasculopathy (including one case of thrombotic microangiopathy) were found to be accompanied by scleroderma. Chrabaszcz et al. concluded that the most specific renal condition associated with systemic sclerosis is the scleroderma renal crisis, characterized by acute onset of renal failure and severe hypertension. Hence, increasing doses of angiotensin-converting enzyme inhibitors, in addition to other antihypertensive drugs are required for controlling hypertension in such cases.
In our study, we encountered a single case of crystal-induced nephropathy, in a case of sarcoidosis. Intratubular precipitation of crystals leads to tubular obstruction and thereby acute kidney injury. Crystal-induced acute kidney injury most commonly occurs as a result of acute uric acid nephropathy and after administration of poorly soluble drugs, toxins, or metabolites. Certain drugs or medications may be metabolized to insoluble products such as oxalate (ethylene glycol, Vitamin C), leading to the precipitation of calcium oxalate crystals within tubular lumens and causing kidney injury.
Our study had a few limitations. The study size was small, and hence, it is difficult to extrapolate the results to a larger non-SLE rheumatology population. Owing to the retrospective design, it was difficult to assess the cause-effect relationship between rheumatologic diseases and renal lesions. Further prospective studies with a larger sample size are required to elucidate this.
| Conclusion|| |
The most common non-SLE rheumatologic disease found in the study was AAV and the most common histological pattern was pauci-immune crescentic glomerulonephritis. This review elaborates on a broad spectrum of renal histopathological lesions in typical rheumatic diseases as they demonstrate a close relationship, thus trying to amalgamate and combine information that is scattered in the literature. Renal involvement can be caused by the usage of anti-rheumatic drugs or the rheumatic disease itself; hence, a more effective and thoughtful approach for definitive diagnosis is needed so that accurate treatment and proper care are warranted for the benefit of the patient.
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Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2]
[Table 1], [Table 2], [Table 3]