|Ahead of print publication
Clinical profile and outcome of antineutrophil cytoplasmic antibody-associated vasculitis: A retrospective observational study from South India
Sham Santhanam1, Hema Murugesan2, Kavitha Mohanasundaram3
1 Department of Rheumatology, Gleneagles Global Health City, Chennai, Tamil Nadu, India
2 Department of Rheumatology, Stanley Medical College, Chennai, Tamil Nadu, India
3 Department of Rheumatology, Saveetha Medical College, Thandalam, Tamil Nadu, India
|Date of Submission||24-Oct-2021|
|Date of Acceptance||06-Mar-2022|
|Date of Web Publication||06-Jul-2022|
Department of Rheumatology, Saveetha Medical College, Thandalam, Tamil Nadu
Source of Support: None, Conflict of Interest: None
Aim: The aim was to study the clinical profile and outcome of patients with antineutrophil cytoplasmic antibody-associated vasculitis (AAV).
Methods: This was a retrospective observational study of patients with a diagnosis of AAV (granulomatosis with polyangiitis [GPA], microscopic polyangiitis [MPA], and eosinophilic granulomatosis with polyangiitis [EGPA]). Patient records from January 2015 to December 2020 were retrieved and included in the analysis. We used the European Medicines Agency (EMA) algorithm for classification of patients.
Results: Forty (14 males and 26 females) patients were included (34 – GPA, 4 – MPA, and 2 – EGPA). The median age was 48 years (54.5 – males and 46 – females). The median disease duration was 6 months, and the median follow-up duration was 18.5 months. As per European Vasculitis Society disease categorization, 25 had organ/life-threatening type, 10 had rapidly progressive renal failure/pulmonary hemorrhage, 4 nonorgan threatening, and 1 refractory disease. The median erythrocyte sedimentation rate (mm/h) and C-reactive protein (mg/L) were 64 and 52.49, respectively. The median Birmingham Vasculitis Activity Score was 15.5. Twenty-six had constitutional features, 22 musculoskeletal, 24 pulmonary, 19 renal, 13 ocular, 13 ENT involvement, 10 mucocutaneous, 11 peripheral nervous system, 1 central nervous system, and 3 had cardiovascular involvement. As induction therapy, cyclophosphamide was used in 15 and rituximab in 20 patients.
Conclusion: The age of onset of AAV was relatively delayed in comparison to other Indian studies. We had female predominance similar to other Indian studies but in contrast to European and US cohorts. In comparison to other Indian studies, prevalence of ENT and ocular manifestations were less and none of the subjects had gastrointestinal involvement.
Keywords: Antineutrophil cytoplasmic antibody clinical profile, cyclophosphamide granulomatosis with polyangiitis, outcome, rituximab
|How to cite this URL:|
Santhanam S, Murugesan H, Mohanasundaram K. Clinical profile and outcome of antineutrophil cytoplasmic antibody-associated vasculitis: A retrospective observational study from South India. Indian J Rheumatol [Epub ahead of print] [cited 2022 Aug 20]. Available from: https://www.indianjrheumatol.com/preprintarticle.asp?id=350019
| Introduction|| |
Antineutrophil cytoplasmic antibody (ANCA)-associated vasculitis (AAV) is a predominant small vessel vasculitis comprising granulomatosis with polyangiitis (GPA, previously known as Wegener's granulomatosis), microscopic polyangiitis (MPA), eosinophilic granulomatosis with polyangiitis (EGPA, previously known as Churg–Strauss syndrome), and drug-induced ANCA vasculitis. ANCA plays a major role in the pathogenesis by activating neutrophils and causing vessel injury. The common organs involved are the lungs, kidneys, paranasal sinuses, eyes, nerves, skin, and the gastrointestinal system.
Watts et al. proposed the European Medicines Agency (EMA) algorithm for classification of AAV and polyarteritis nodosa. The entry criterion is to have features of primary systemic vasculitis and then a stepwise classification is made. One of the advantages is minimization of patients with unclassifiable vasculitis.
The first case report and case series from India was published by Singh et al. way back in 1985. Since then, various case series have been published, with Kumar et al. publishing a series of 45 patients with GPA in 2015. In 2017, Sharma et al. published the largest case series from India of 105 patients with GPA. A comprehensive list of studies on chronological order in AAV from India was discussed by Handa. A recent addition to the studies on AAV from India is one on epidemiology and a proposed genetic model to help in early diagnosis and prognosis.
Although we have studies on ANCA vasculitis reported from India, there are only a few studies from South India., In 2018, Nunna et al. reported a series of 31 patients with ANCA vasculitis and the same year Shobha et al. published a study of 60 patients with GPA., To the best of our knowledge, there are very few studies from our state (Tamil Nadu) except for one by Chandrasekaran et al. in 1995 and one abstract published by Rajappa in 2002.,
In view of limited available data, we did this retrospective observational study analyzing the clinical characteristics, laboratory features, side effects, and treatment outcome of patients with AAV. We tried to analyze the differences in clinical characteristics between studies from Northern and Southern India and in comparison to the West.
| Methods|| |
This was a retrospective observational study of patients being treated at the rheumatology department of three tertiary care hospitals. The medical records of both outpatients and inpatients over the past 6 years (January 2015 till December 2020) were analyzed. Patients with a diagnosis of ANCA-associated vasculitis (GPA, MPA, and EGPA) were screened. The EMA algorithm was used for stepwise classification of these patients to minimize unclassifiable patients.
A detailed history, clinical examination, routine blood investigations (hemogram, inflammatory markers, renal function test, liver function test, urine routine, and urine protein–creatinine ratio), chest radiography, echocardiography, and high-resolution computed tomography chest were studied at baseline and during follow-up (as and when required). Reports of ANCA testing done by indirect immunofluorescence (IIF) and enzyme-linked immunoassay (ELISA) (anti-proteinase 3 [PR3] and anti-myeloperoxidase [MPO] antibody [Ab]) were included. Other relevant investigations such as tissue biopsy (renal, skin, lung, and paranasal sinuses) and imaging (magnetic resonance imaging and coronary angiogram) were noted.
Disease staging and disease activity assessment
The disease staging (nonorgan threatening, organ or life threatening, rapidly progressive glomerulonephritis [RPGN]/diffuse alveolar hemorrhage [DAH]) was done as per the European League Against Rheumatism/European Vasculitis Society (EUVAS) disease staging for ANCA-associated vasculitis. The disease activity was calculated by Birmingham Vasculitis Activity Score version 3 (BVAS 3). Patients with a BVAS score of 0 were considered to be in remission. Outcome was calculated for patients on treatment and with a minimum follow-up of 6 months. The number of deaths and the clinical characteristics of those patients were analyzed.
Written and informed consent was obtained from all the study participants in compliance with the Helsinki Declaration. The study was performed in accordance with the ethical standards of institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments and comparable ethical standards.
The study was approved by the Institutional Ethics Committee for Biomedical Health and Research, Gleneagles Global Health City vide letter number EC/NEW/ INST–BMHR/2020/004 dated 05/09/2020.
For continuous data, the median and interquartile range were computed, and for categorical data, percentage and proportion were calculated.
| Results and Analysis|| |
We screened a total of 40 patients, and all of them were classifiable as AAV according to the EMA algorithm and were included in the study. Hence, all the forty patients were included, with 34 diagnosed as GPA, 4 as MPA and 2 as EGPA. The classification of patients as per EMA algorithm is depicted as a flowchart [Figure 1]. All the clinical characteristics of the study population are discussed and classified as per BVAS disease categorization in [Table 1]. Majority were females (female: male ratio – 1.8:1); the median age of presentation was higher in males. The median duration of follow-up was 18.4 (3–72) months. Majority of the patients had organ or life-threatening disease followed by patients with RPGN/DAH [Table 1]. Constitutional symptoms including musculoskeletal involvement were common (65%), followed by pulmonary (60%) and renal (47.5%) involvement. None of the patients had involvement of gastrointestinal system.
|Table 1: Clinical characteristics of the study population during the course of the disease|
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|Figure 1: Patients who satisfied the entry criteria for a clinical diagnosis of antibody-associated vasculitis (antineutrophil cytoplasmic antibody-associated vasculitis) were classified stepwise according to European Medicine Agency algorithm, GPA: Granulomatosis with polyangiitis, MPA: Microscopic polyangiitis, EGPA: Eosinophilic granulomatosis with polyangiitis, ACR: American college of rheumatology, CHCC: Chapel hill consensus conference |
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We had two patients with EGPA; one presented with constitutional symptoms, lung infiltrates, pauci-immune glomerulonephritis, mononeuritis multiplex, and cardiomyopathy; the second patient presented with constitutional symptoms and mononeuritis multiplex. Both had hypereosinophilia but had no symptoms suggestive of asthma or sinusitis, and they tested positive for both p-ANCA by IIF and anti-MPO Ab by ELISA.
Four patients were diagnosed with MPA. They had a mean age of 68.75. All tested positive for anti-MPO antibodies by ELISA and for p-ANCA by IIF. Three of them had diffuse alveolar hemorrhage, 3 had rapidly progressive glomerulonephritis of which 2 had pulmonary renal syndrome.
Among the 34 GPA patients, one 16-year-old female had presented initially with cutaneous vasculitis and arthritis and later progressed to renal involvement. On renal biopsy, she had pauci-immune crescentic glomerulonephritis and tested negative for ANCA both by IIF and ELISA. She was included in the analysis considering the typical biopsy findings.
Some of the rare manifestations of GPA in our study group were hypophysitis, bronchial stenosis, subglottic edema, organizing pneumonia (OP), isolated 7th and 8th nerve palsies, and involvement of coronary arteries. The patient-related clinical and radiographic images are depicted in [Figure 2] and [Figure 3], and the details are mentioned in [Table 1].
|Figure 2: (a and b) A 29-year-old female with granulomatosis with polyangiitis – chest radiograph and high-resolution computed tomography of chest of revealing nodules in both the right lung and the left lung. (c) A 63-year-old male with granulomatosis with polyangiitis – presenting with cryptogenic organizing pneumonia. (d) A 50-year-old female with granulomatosis with polyangiitis – presented with right bronchial stenosis|
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|Figure 3: (a) A 23-year-old female with granulomatosis with polyangiitis presented with cutaneous gangrene of both hand and foot. (b) A 73-year-old male with microscopic polyangiitis – chest radiography suggestive of diffuse alveolar bleed. (c and d) Granulomatosis with polyangiitis patient with infiltrates and fibrosis of the lung before (c) and after (d) treatment with cyclophosphamide|
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The details of ANCA positivity, inflammatory markers, and tissue biopsy findings are discussed in [Table 2]. Majority of the patients tested positive for ANCA by both IIF and ELISA. One patient had tested positive for both anti-MPO Ab and anti-glomerular basement membrane (GBM) Ab. Sixteen patients underwent a tissue biopsy, of which two patients had normal paranasal sinus biopsy and one each had a normal lung and renal biopsy. All the remaining had positive finding in biopsy contributing to the diagnosis.
|Table 2: Disease activity, laboratory investigations, and tissue biopsy details of the study population|
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During induction therapy, all 40 patients were treated with steroids. Twenty-five of them were treated with pulse steroids initially followed by oral steroids. Fifteen patients were treated with cyclophosphamide (as first line in 14 and second line in 1) and 20 patients with rituximab (as first line in 18 and second line in 2). Plasma exchange (PLEX) was used in seven patients during induction therapy, of which five improved and two died. Four of them had RPGN/DAH, two had organ/life-threatening disease, and one had refractory disease. All of them had severe renal involvement and/or DAH. Mycophenolate mofetil was used as induction therapy in three patients and in another two as add-on drug to rituximab. Methotrexate was used in two patients as induction therapy. During maintenance therapy, four patients were on rituximab (500 mg once in 6 months), 11 were on azathioprine, 8 on mycophenolate mofetil, and one was on methotrexate.
Treatment and outcome
Mortality was 10% (4/40). Two of them had GPA and two had MPA. One of the MPA patients tested positive for both anti-MPO Ab and anti-GBM Ab. Three patients presented with pulmonary renal syndrome and one with alveolar bleed. All the three patients with pulmonary renal syndrome were treated with intravenous pulse steroids and PLEX followed by intravenous cyclophosphamide in two of them. One patient with alveolar bleed was treated with intravenous pulse steroids and rituximab. Both the GPA patients were refractory to treatment and died during first admission. One MPA patient with dual Ab positivity was on maintenance hemodialysis and died by 3 months. The MPA patient treated with rituximab succumbed to lung infection (rhinovirus and enterovirus isolated from bronchoalveolar lavage) by 18 months.
Two (2/40) patients with GPA lost follow-up after a period of 3 months.
Nine patients (9/34) were in the phase of induction therapy and yet to complete 6 months of follow-up. The remaining 25 (25/34) patients had minimum of 6-month follow-up. Fifteen patients attained complete remission, four had relapse, and two patients (GPA) improved but had persistent lung nodules on imaging. Four patients (3 – GPA and 1 – MPA) had chronic kidney damage on maintenance hemodialysis awaiting renal replacement therapy.
Four patients with GPA relapsed and all of them had a major relapse (2 – alveolar hemorrhage, 1 – renal, and 1 – scleritis). Two of them had cyclophosphamide and rituximab for induction therapy. On relapse, they were alternatively induced with rituximab or cyclophosphamide. One patient on rituximab relapsed with recurrence of scleritis, and on adding MMF, she went into remission. Another patient was treated suboptimally with cyclophosphamide 4 years back and on relapse was again induced with intravenous cyclophosphamide as per CYCLOPS regimen and improved. Both the patients with alveolar hemorrhage defaulted treatment; one with renal relapse was treated prior with a suboptimal dose of immunosuppressive, and there was no identifiable risk factor in the patient with relapse of scleritis.
Close to one-fourth (~25% [9/40]) of the patients had infections. One GPA patient on steroids and intravenous cyclophosphamide developed infected pancreatic pseudocyst which had to be drained. Another patient succumbed to viral pneumonia with bronchoalveolar lavage growing rhinovirus and enterovirus. Two patients on cyclophosphamide developed bacterial pneumonia necessitating inpatient management. The remaining five had upper respiratory tract infections managed as outpatients.
We had 11 (27.5%) patients who got vaccinated with both influenza and pneumococcal vaccines. Stable patients were vaccinated initially, but majority of them were vaccinated during follow-up once the disease activity was controlled.
Adverse effects due to drugs
Two patients developed leukopenia: one patient was on cyclophosphamide and the other was on azathioprine. One patient developed steroid-induced cataract and diabetes mellitus. One patient had chills and rigors during rituximab infusion and settled with antihistamines and steroids.
| Discussion|| |
The current study was a retrospective observational study of patients with AAV and one of the few studies from South India. Forty (34 – GPA, 4 – MPA, and 2 – EGPA) patients were included. We had compared the clinical characteristics of our study with other studies from Southern and Northern India and also with studies from the West [Table 3]. The median age group of presentation in our cohort was relatively late in comparison to other Indian studies. Females out-numbered males in our cohort; the pattern was similar to other Indian studies but in contrast to European and US cohorts. The incidence of constitutional, pulmonary, renal, and musculoskeletal manifestations in our cohort was similar to other Indian studies; ENT and ocular involvement were less in our study.
|Table 3: Comparing the clinical characteristics, serology, and outcome of our study with other studies done from India, the United states, and Europe|
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In 2017, Sharma et al. published their experience on pulmonary and ENT manifestations of AAV from a tertiary care center in North India. They had a cohort of 92 patients, with 76% of the patients having clinical or radiological evidence of lung involvement. DAH was present in 60% of MPA patients and 10.1% of GPA patients. Fifty-nine percent of patients had ENT involvement; it was more common in GPA. In 2018, Majumder et al. reported a case series of 26 patients with isolated scleritis who tested positive for ANCA, of which eight patients had a diagnosis of GPA; three patients had scleritis as the initial presentation.
We analyzed the various case series published from India and tried to look into the clinicodemographic difference between studies from Northern and Southern India. The incidence of lung and kidney involvement was similar across studies; our cohort did not have any patient with gastrointestinal involvement. We could not find any major differences except for reduced ENT involvement in the two studies (our study and Shobha et al.) from South India, unlike the study by Nunna et al. The possible reasons are as follows: (1) majority of the patients presented with organ/life threatening or RPGN/DAH class with only a few having non-organ threatening or limited type and (2) may be related to the referral pattern at each center. At our centers, the majority of the referrals were from the pulmonology department and intensive care unit.
Naidu et al. studied the difference in clinical characteristics of GPA in Asia from the West. They found that MPA was more common in Asian countries (Japan and China) and GPA in Northern Europe. In India, we do not have studies estimating the prevalence of AAV. The mean age of disease onset in India was 40 years (delayed in our cohort) in comparison to 65 years in Japan. In China and Japan, 60% of GPA patients were anti-MPO positive, but in India and Korea, majority of the GPA patients were anti-PR3 positive. There was a lower frequency of renal involvement in Indian studies in comparison to studies from China and the West.
Recently, Singh et al. reported 42 cases of GPA from a single tertiary care center in Western India. The median age was 48.5 years with an equal number of males and females. The median BVAS was 14.5. Pulmonary manifestations were common followed by ENT and renal involvement. Three out of 36 patients expired and 17 patients had relapse. Rituximab was found to be effective in treating relapse, refractory, and severe disease.
In our study, two patients presented with fever and hemoptysis; they had organizing pneumonia (OP) and tested positive for anti-MPO Ab with high titer values (>200 units by ELISA). There are case reports of ANCA vasculitis presenting with OP or isolated anti-MPO Abs (without vasculitis features) in patients with OP. Uner et al. reported a case series of Wegener's granulomatosis patients presenting with bronchiolitis obliterans-organizing pneumonia-like variant.
One patient with GPA had associated interstitial lung disease with c-ANCA positivity. Pulmonary involvement is common with GPA and MPA. MPA patients with pulmonary fibrosis had less severe inflammatory response with reduced frequency of kidney and lung involvement. Pulmonary fibrosis can occur concurrently or can precede (similar to our patient) the onset of AAV. Usual interstitial pneumonia is the frequent type reported. Prevalence of ILD is more with MPA (2.7%–45%) than GPA (23%), and the most common Ab associated is anti-MPO Abs.
In our study, three patients with a diagnosis of rheumatoid arthritis (clinically and serologically) initially developed AAV with anti-MPO Ab positivity later. Mustila et al. studied 246 patients with RA and found 21% of patients with p-ANCA positivity. They concluded that with p-ANCA positivity, there is an increase in inflammatory activity and also an increased risk for RA nephropathy. Draibe and Salama reported the association of AAV with RA as a lesser diagnosed overlap syndrome.
One of the MPA patients who presented with pulmonary renal syndrome had dual positivity for anti-MPO Abs and anti-GBM Abs. A single-center study on dual-positive ANCA and anti-GBM reported a higher incidence of lung hemorrhage in that group and 82% had anti-MPO antibodies. Increased incidence of crescentic glomerulonephritis was noted and renal outcome was poor in that group. Our patient also had antibodies directed against MPO.
In a study by McAdoo et al., they analyzed patients with isolated ANCA positivity, isolated anti-GBM Ab positivity, and dual positivity for both antibodies. Double-positive patients behave more like anti-GBM disease initially and have a higher incidence of lung hemorrhage. However, the overall survival was similar between the three groups. Advanced age, severe renal failure, and pulmonary hemorrhage were considered poor prognostic factors in that study.
Our patient had all the three risk factors and died by 3 months. Hence, double-positive patients need aggressive induction therapy for anti-GBM disease with close follow-up and long-term maintenance therapy for AAV.
Our study has few limitations. First, it was a retrospective observational study; we were not able to capture all the data. We did not report the mean steroid dosage during maintenance phase. Vasculitis damage index was not calculated. We did not assess the risk factors for infection. The sample size was small and the follow-up duration was relatively less in comparison to other Indian studies. The possibility of referral bias needs to be considered as all were tertiary care centers accounting for the high disease activity and severity at presentation.
| Conclusion|| |
Our study will add to the existing data on AAV from India. We had predominant GPA patients with the age of onset slightly delayed in comparison to other Indian studies. We had female predominance similar to other Indian studies but in contrast to the West. In comparison to other Indian studies, prevalence of ENT and ocular manifestations were less with no reports of GI involvement. Majority of the patients in our study cohort had organ/life threatening or RPGN/DAH class according to EUVAS category.
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Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2], [Table 3]